Mechanisms and ecological implications of the movement of bacteria in soil

doi:10.1016/j.apsoil.2018.04.014

Applied Soil Ecology

Volume 129, August 2018, Pages 112-120

https://doi-org.remotexs.ntu.edu.sg/10.1016/j.apsoil.2018.04.014 Get rights and content

Highlights

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In soil, air-filled pores between soil particles restrict bacterial dispersal.
在土壤中，土壤颗粒之间充满空气的孔隙限制了细菌的传播。
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Passive transport of bacterial cells in soil occurs mainly by wind or flowing water.
细菌细胞在土壤中的被动运输主要通过风或流动的水进行。
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Key bacterial transport mechanisms are truck-like and network-assisted mechanisms.
关键的细菌运输机制是类似卡车和网络辅助的机制。
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Dispersal in soil allows key bacteria to extend their sphere of influence.
土壤中的扩散使关键细菌得以扩大其影响范围。

Abstract

The extent of translocation of bacteria through soil strongly affects parameters of bacterially-mediated bioremediation and biocontrol. Here, we discuss the main strategies that bacteria use for their dispersal through the soil matrix. Cell dispersal mechanisms are scale-dependent and may be either growth- or cell organelle-driven (active, small scale) or water/wind/vector-organism-driven (passive, large scale). The active modes of dispersal (growth, swimming, swarming and twitching motility) are limited to the scale of (connected) soil pores or aggregates. In contrast, water- or wind-driven transport dominates large-distance bacterial dispersal. Remarkably, the association of bacteria with other (vector) organisms, in particular plant roots, fungal hyphae and moving organisms like earthworms, assists them in the crossing of soil matrix discontinuities. We posit that a dynamic “underground transport web” exists in soil, which is organism- (plant-, fungal- and/or soil animal-) driven. In particular, we examine the role of fungal hyphae as facilitators of short- or long-distance bacterial migration through soil. The transport web thus has strong implications for the occupancy of novel ecological niches and nutrient cycling dynamics. The effects of this underground transport web are examined.
细菌通过土壤的迁移程度强烈影响细菌介导的生物修复和生物控制的参数。在此，我们讨论了细菌在土壤基质中传播的主要策略。细胞传播机制是依赖于尺度的，可能是由生长或细胞器驱动的（主动，小尺度）或由水/风/载体生物驱动的（被动，大尺度）。主动传播模式（生长、游动、群体运动和抽动运动）仅限于（连接的）土壤孔隙或聚集体的尺度。相比之下，水或风驱动的运输主导了远距离的细菌传播。值得注意的是，细菌与其他（载体）生物，特别是植物根、真菌菌丝和像蚯蚓这样的移动生物的关联，帮助它们跨越土壤基质的不连续性。我们假设在土壤中存在一个动态的“地下运输网”，这是由生物（植物、真菌和/或土壤动物）驱动的。特别是，我们研究了真菌菌丝在促进细菌通过土壤进行短距离或长距离迁移中的作用。因此，运输网络对新生态位的占据和养分循环动态有着重要影响。本文将探讨这一地下运输网络的影响。

Keywords

Bacterial motility

Fungal highway

Plant rhizosphere

Dispersal

1. Introduction – The importance of bacterial dispersal for differentiation processes and soil functioning

Numerous studies have demonstrated that soil constitutes a key reservoir of biological entities that – together – exhibit enormous diversity. Next to plants and larger soil (in)vertebrates, this reservoir includes populations of bacteria, fungi, protozoa, nematodes, earthworms and arthropods (Bardgett and van der Putten, 2014, Bender et al., 2016). Across this complex biota, bacteria – in the light of their extremely high numbers – stand out as key soil inhabitants. Bacteria are the prime players in the soil biogeochemical cycles, such as those of carbon, nitrogen, sulfur and phosphorus (Long et al., 2016). These cycles are crucial for soil fertility, as they recycle materials and provide nutrients for plant growth. Bacteria are also involved in bioremediation processes in cases of soil pollution. However, due to their small cell sizes, bacteria act within very small spheres of influence (Kuzyakov and Blagodatskaya, 2015), requiring dispersal mechanism(s) to broaden their zones of influence across the soil. The nature of the soil matrix clearly places strong limits to bacterial spread (Griffin and Quail, 1968, Vanapalli et al., 1999). We here examine how such bacterial dispersal through soil can take place, i.e. via either active or passive processes, or by a combination of these two.
大量研究表明，土壤是生物实体的重要储存库，这些生物实体共同展示了巨大的多样性。除了植物和较大的土壤（无）脊椎动物外，这个储存库还包括细菌、真菌、原生动物、线虫、蚯蚓和节肢动物的种群（Bardgett 和 van der Putten, 2014，Bender 等, 2016）。在这个复杂的生物群中，细菌由于其数量极多，成为土壤中的主要居民。细菌是土壤中碳、氮、硫和磷等生物地球化学循环的主要参与者（Long 等, 2016）。这些循环对土壤肥力至关重要，因为它们回收材料并为植物生长提供养分。细菌还参与土壤污染情况下的生物修复过程。然而，由于细菌的胞体大小较小，它们的影响范围也很小 (Kuzyakov and Blagodatskaya, 2015)，因此需要扩散机制来扩大它们在土壤中的影响范围。土壤基质的性质显然对细菌扩散有很大的限制 (Griffin and Quail, 1968, Vanapalli et al., 1999)。我们在此研究细菌在土壤中的扩散如何发生，即通过主动或被动过程，抑或这两者的结合。

Depending on nutrient supply (Banitz et al., 2012) and predation pressure (Otto et al., 2017a), active bacterial movement along surfaces can occur in a variety of ways (Henrichsen, 1972, Jarrell and McBride, 2008). Thus, under proper conditions of nutrient supply, bacteria can actively reach remote sites by: (i) flagellum-driven swimming motility (over a surface with a sufficiently thick fluid film), and/or (ii) swarming motility (at a surface with a limited fluid layer). Often, chemotaxis is involved, determining directional movement (Furuno et al., 2010, Haq et al., 2016). In addition, so-called twitching motility driven by type four pili (T4P) may take place. Twitching is highly localized, as driven by the extension and retraction of T4 pilus proteins. Another type of (pilus/flagellum-independent) movement, called gliding motility, can occur on specific surfaces in the soil matrix. Gliding motility relies on the presence of a focal adhesion complex which allows bacterial cells to glide over a relatively dry, hard surface (Nan and Zusman, 2011). Lastly, researchers have recently found (Park et al., 2015, Shrout, 2015), in experiments on agar surfaces, that bacterial cells can be “pushed” forward by expansive force in a growing colony. In the process, cells delay their timing of septum formation and division, with the concomitant action of surfactants. This type of motility has been denominated sliding motility. Here, one should notice that the active migration processes are energy-expensive, and so particular “nutrient-rich” or “nutrient-sufficient” conditions need to exist in the soil to make active migration successful. Additionally, low levels of predation pressure have been found to promote bacterial translocation along dispersal networks (Otto et al., 2017a). However, it is not yet understood to what extent and under which conditions this process operates in soil settings; very likely, it is important in short-distance movement.
根据营养供应（Banitz et al., 2012）和捕食压力（Otto et al., 2017a），活跃的细菌沿表面移动可以通过多种方式发生（Henrichsen, 1972，Jarrell and McBride, 2008）。因此，在适当的营养供应条件下，细菌可以通过以下方式主动到达远处地点：（i）鞭毛驱动的游动能力（在具有足够厚液膜的表面上），和/或（ii）群集运动能力（在具有有限液层的表面上）。通常，趋化性参与其中，决定方向性运动（Furuno et al., 2010，Haq et al., 2016）。此外，所谓的由四型菌毛（T4P）驱动的抽动运动也可能发生。抽动运动高度局部化，由 T4 菌毛蛋白的延伸和收缩驱动。另一种（不依赖菌毛/鞭毛的）运动，称为滑行运动，可以在土壤基质的特定表面上发生。滑行运动依赖于一个焦点粘附复合体的存在，使细菌细胞能够在相对干燥、坚硬的表面上滑行（Nan 和 Zusman, 2011）。最后，研究人员最近在琼脂表面上的实验中发现（Park 等, 2015，Shrout, 2015），细菌细胞可以通过在生长菌落中的膨胀力“推动”向前。在此过程中，细胞延迟了隔膜形成和分裂的时间，同时伴随着表面活性剂的作用。这种运动类型被称为滑动运动。在这里，需要注意的是，主动迁移过程是耗能的，因此土壤中需要存在特定的“富营养”或“营养充足”条件才能使主动迁移成功。此外，低捕食压力被发现可以促进沿扩散网络的细菌转移(Otto et al., 2017a)。然而，目前尚不清楚这种过程在土壤环境中在何种程度和何种条件下运行；很可能在短距离移动中很重要。

In addition to the afore-discussed active modes of bacterial cell spread along surfaces, cells can be moved passively in soil, e.g. along with water flowing through soil (Hekman et al., 1995) or even by blowing wind [in dry top soils] (Kellogg and Griffin, 2006). A suite of previous studies and reviews have addressed the translocation of bacterial cells with water flow through soil (Breitenbeck et al., 1988, Hekman et al., 1995, Stevik et al., 2004), and hence this type of movement will not be extensively discussed in this paper. Rather, we will place a focus on organism-driven transport modes, as discussed in the following.
除了前面讨论的细菌细胞沿表面扩散的主动模式外，细胞还可以在土壤中被动移动，例如随着水流通过土壤 (Hekman et al., 1995) 或者甚至被吹风带动 [在干燥的表土中] (Kellogg and Griffin, 2006)。一系列先前的研究和综述已经探讨了细菌细胞随水流通过土壤的转移 (Breitenbeck et al., 1988, Hekman et al., 1995, Stevik et al., 2004)，因此本文不会对这种类型的运动进行广泛讨论。相反，我们将重点放在由生物体驱动的运输模式上，如下所述。

Several recent studies have revealed that specific bacterial types possess capacities to “hitchhike” along with other (vector) organisms through the soil. Such vector organisms range from protozoa, nematodes and earthworms to soil fungi and plant root systems (Daane et al., 1996, Kohlmeier et al., 2005, Warmink and van Elsas, 2009, Glaeser et al., 2016), and soil physicochemical parameters are important determinants of the movement.
最近的几项研究表明，特定类型的细菌具备与其他（载体）生物一起“搭便车”通过土壤的能力。这些载体生物从原生动物、线虫和蚯蚓到土壤真菌和植物根系（Daane 等, 1996、Kohlmeier 等, 2005、Warmink 和 van Elsas, 2009、Glaeser 等, 2016），土壤的物理化学参数是这种运动的重要决定因素。

We here first examine the conditions in soil that critically affect the motility of bacterial cells in soil. Then, we address the prevailing types of bacterial motility as related to soil conditions. We examine to what extent these, depending on the soil ecological context, drive bacterial dispersal. Moreover, we propose a revision of the classical theory that posits that bacteria are largely confined to their microhabitats in soil and will only travel longer distances when driven by water, wind and moving soil organisms like earthworms (Hekman et al., 1995, Daane et al., 1996, Kellogg and Griffin, 2006). In the revision, fungal hyphae are also key actors in bacterial transportation, as they provide “highways” along which bacterial cells may travel, passively and/or actively. An “underground transport web” is thus proposed to exist, which is dynamic and includes fungal hyphal networks, plant roots and earthworms, and interconnections between these. This transport web is perceived to broaden the translocation possibilities of particular bacteria through the soil matrix, which may directly affect soil processes in cases where establishment of such migrated bacterial cells in novel soil microhabitats is possible. Finally, we examine the potential ecological effects of bacterial dispersal in soil. On the basis of these analyses, a novel framework for bacterial movement through soil is proposed.
我们首先研究了土壤中严重影响细菌细胞运动性的条件。然后，我们讨论了与土壤条件相关的主要细菌运动类型。我们研究了这些在多大程度上根据土壤生态环境驱动细菌扩散。此外，我们提出修订经典理论，该理论认为细菌主要局限于其在土壤中的微生境，只有在水、风和移动的土壤生物如蚯蚓的驱动下才会长距离移动（Hekman et al., 1995，Daane et al., 1996，Kellogg and Griffin, 2006）。在修订中，真菌菌丝也是细菌运输的关键角色，因为它们提供了细菌细胞可以沿着其被动和/或主动移动的“高速公路”。因此，提出存在一个“地下运输网络”，该网络是动态的，包括真菌菌丝网络、植物根系和蚯蚓，以及它们之间的相互连接。这种运输网络被认为可以通过土壤基质扩大特定细菌的转移可能性，在这些迁移的细菌细胞能够在新的土壤微生境中建立的情况下，可能直接影响土壤过程。最后，我们研究了细菌在土壤中扩散的潜在生态影响。基于这些分析，提出了一个细菌在土壤中移动的新框架。

2. Bacterial dispersal is affected by the soil pore network and water properties

Moisture content is an essential factor that mediates bacterial cell motility in soil, with bacterial cells having greater possibilities to migrate with increasing soil water content. For instance, Pseudomonas aeruginosa Migula was shown to move 20 mm in 24 h in soil under relatively wet, but not under dry conditions (Griffin and Quail, 1968). The level of connectivity of the water-filled (versus air-filled) pores in the soil has been invoked as an explanatory factor influencing cell motility, with the liquid phase being discontinuous in water-unsaturated soil (Vanapalli et al., 1999). Thus, the air-filled pores between soil particles represent structural discontinuities that impair cell motility, while the ones that are filled with water bridge the gaps. With respect to what they do for the 0.5–2 μm soil bacteria, the pores in the soil matrix have been classified on the basis of the pore size (defined as equivalent cylindrical diameter, ECD, which is computed from the cylindrical capillary rise), into transmission pores (60 < ECD < 600 μm), coarse storage pores (6 < ECD <60 μm), fine storage pores (0.2 < ECD < 6 μm) and residual pores (ECD < 0.2 μm) (Hayashi et al., 2006). In this depiction, transmission and coarse storage pores have dimensions that greatly exceed those of the majority of bacterial cells. If not water-filled, these effectively impair cell passage. Bacterial cells may largely find shelter inside the so-called storage pores. Clearly, the soil pore size distribution exerts a critical overall influence on (active and passive) bacterial motility in soil. In contrast to actual pore median size, pore neck sizes are important; pores with necks equal to, or lower than, bacterial cell sizes, are likely to restrict the rate of bacterial movement (Andreoglou et al., 2003).
含水量是调节土壤中细菌细胞运动的一个重要因素，随着土壤含水量的增加，细菌细胞迁移的可能性更大。例如，铜绿假单胞菌 Migula 在相对湿润的土壤中 24 小时内移动了 20 毫米，但在干燥条件下则没有移动 (Griffin 和 Quail, 1968)。土壤中充水孔隙（相对于充气孔隙）的连通性水平被认为是影响细胞运动的解释因素，在水分不饱和的土壤中液相是不连续的 (Vanapalli 等, 1999)。因此，土壤颗粒之间的充气孔隙代表了阻碍细胞运动的结构不连续性，而充水孔隙则弥合了这些间隙。至于它们对 0 的作用。5–2 μm 土壤细菌，土壤基质中的孔隙根据孔隙大小（定义为等效圆柱直径，ECD，通过圆柱毛细上升计算得出）被分类为传输孔隙（60 < ECD < 600 μm）、粗储存孔隙（6 < ECD <60 id=113>Hayashi et al., 2006）。在这种描述中，传输孔隙和粗储存孔隙的尺寸远大于大多数细菌细胞的尺寸。如果没有充满水，这些孔隙会有效地阻碍细胞通过。细菌细胞可能主要在所谓的储存孔隙中找到庇护。显然，土壤孔隙大小分布对土壤中细菌的（主动和被动）运动具有关键的整体影响。与实际孔隙中值大小相比，孔隙颈部大小更为重要；孔隙颈部大小等于或小于细菌细胞大小的孔隙，可能会限制细菌运动的速度（Andreoglou et al., 2003）。

The pore size distribution is intrinsically linked to the soil textural type, with a coarser (sandy) soil having a larger proportion of large pores when compared to a finer (clay) soil. Thus, soil texture directly affects bacterial motility in soil, first on the basis of the soil pore network characteristics and secondly due to the forces of attraction exerted by the soil surfaces that bacterial cells are exposed to (MacDonald and Duniway, 1978). In order to translocate in soil, bacterial cells have to resist the attractive forces exerted by soil surfaces. Additionally, soil density (linked to soil compaction) is an important factor that influences bacterial motility in soil. That is, higher soil bulk densities clearly limit the movement of bacterial cells with percolating water (van Elsas et al., 1991). Another issue is the degree of hydrophobicity of soil, which affects its infiltration capacity and subsequently the three-dimensional distribution and dynamics of soil moisture (Doerr et al., 2000). This also influences the formation of water films in soil, as well as the water connectivity (Goebel et al., 2011) and bacterial dispersal.
孔径分布与土壤质地类型有内在联系，较粗的（沙质）土壤相比较细的（粘土质）土壤拥有较大比例的大孔径。因此，土壤质地直接影响土壤中细菌的运动，一方面基于土壤孔隙网络的特性，另一方面由于细菌细胞暴露的土壤表面所施加的吸引力（MacDonald 和 Duniway, 1978）。为了在土壤中转移，细菌细胞必须抵抗土壤表面施加的吸引力。此外，土壤密度（与土壤压实相关）是影响土壤中细菌运动的重要因素。也就是说，更高的土壤容重明显限制了细菌细胞随渗透水的运动（van Elsas 等， 1991）。另一个问题是土壤的疏水性程度，它影响其渗透能力，进而影响土壤湿度的三维分布和动态变化（Doerr 等, 2000）。这也影响了土壤中水膜的形成，以及水的连通性（Goebel 等，2011）和细菌的扩散。

3. Bacterial movement through soil

3.1. Active movement

In the presence of water that increases the connectivity of soil micro-aggregates, bacterial cells can move actively via flagellar motility, in addition to their passive translocation as a result of Brownian movement (Griffin and Quail, 1968). In cases flagella are present, the latter type of movement is often overruled (Abu-Ashour et al., 1994). Thus, flagellum-driven chemotaxis was described early-on for the plant growth promoters Azospirillum brasilense and Pseudomonas fluorescens, which both migrated up to 80 mm in soil towards wheat seedlings and synthetic attractants (Bashan, 1986). Conversely, a recent study (in which chemotaxis did not occur) showed that Bradyrhizobium japonicum was able to move randomly up to 7 mm away from its inoculation site in water-saturated soil via flagellar activity (Covelli et al., 2013). Interestingly, much like soil fungi, some bacterial types can form multicellular chain structures, which also support their migration, by sliding motility, through soil. Next to the well-known actinomycetes and Bacillus mycoides, a recent example is given by experiments with Bacillus cereus (strain ATCC14597). Growing cells of this organism can switch to a multicellular phenotype, forming chains and then clumps. These forms can span a considerable distance in soil (tens of micrometers), which results in the overcoming of structural gaps in the soil matrix (Vilain et al., 2006).
在增加土壤微团聚体连通性的水的存在下，细菌细胞除了通过布朗运动被动转移外，还可以通过鞭毛运动主动移动(Griffin and Quail, 1968)。在存在鞭毛的情况下，后一种运动类型通常会被取代(Abu-Ashour et al., 1994)。因此，鞭毛驱动的趋化性早期就被描述为植物生长促进剂巴西固氮螺菌和荧光假单胞菌,，它们在土壤中向小麦幼苗和合成引诱物迁移了多达 80 毫米(Bashan, 1986)。相反，最近的一项研究（其中没有发生趋化性）表明，日本根瘤菌能够通过鞭毛活动在水饱和土壤中随机移动多达 7 毫米远离其接种点(Covelli et al., 2013)。有趣的是，就像土壤真菌一样，一些细菌类型可以形成多细胞链结构，这也通过滑动运动支持它们在土壤中的迁移。除了众所周知的放线菌和粘质沙雷氏菌，最近的一个例子是通过对蜡样芽孢杆菌（菌株 ATCC14597）的实验给出的。这种生物的生长细胞可以切换到多细胞表型，形成链然后聚集。这些形式可以在土壤中跨越相当大的距离（数十微米），从而克服土壤基质中的结构间隙（Vilain et al., 2006）。

3.2. Passive movement

Passive movement through soil can occur due to water flow, wind blows or in connection with organismal vectors. First, water flow through the soil pore network can act as an important mechanism for bacterial cell movement. In several experiments, percolating water has been found to facilitate large-scale/-distance (up to 400 mm) bacterial translocation in soil. Models based on soil physical parameters have been able to describe bacterial cell movement through soil, with bacterial density distributions matching exponential curves depicting cell density decreases with increasing soil depths (Breitenbeck et al., 1988, Hekman et al., 1995). The rate of translocation was thus determined by parameters of the soil pore network, the water flow rate and the number of times the soil was flushed (Trevors et al., 1990, Stevik et al., 2004, Unc and Goss, 2004). Moreover, the contextual soil properties, the initial moisture content and the soil bulk density are also key aspects that drive cell translocations (van Elsas et al., 1991). Intricate models describing water-flow-induced transport are described in several key studies (Beven and Germann, 1982, Hagedorn et al., 2000, Ma et al., 2010), and will not be further discussed here. For the purpose of this review, it suffices to state that the soil textural type, the presence of different clay types and the soil conditions (pH, types of ions present, temperature) are key determinants of adsorption/desorption processes, which affects the degree to which a moving bacterial population can migrate through soil. In nature, rainfall and irrigation provide water flows through soil, albeit irregularly; the extent of water-carried transport is driven by the rules set by the models.
由于水流、风吹或与生物载体的联系，土壤中的被动运动可能发生。首先，通过土壤孔隙网络的水流可以作为细菌细胞运动的重要机制。在几项实验中，渗透水被发现可以促进土壤中大规模/远距离（高达 400 毫米）的细菌转移。基于土壤物理参数的模型能够描述细菌细胞通过土壤的运动，细菌密度分布符合指数曲线，显示出随着土壤深度增加细胞密度减少的趋势（Breitenbeck et al., 1988，Hekman et al., 1995）。因此，转移速率由土壤孔隙网络的参数、水流速率和土壤冲洗次数决定（Trevors et al., 1990，Stevik et al., 2004，Unc and Goss, 2004）。此外，背景土壤特性、初始含水量和土壤容重也是驱动细胞迁移的关键方面（van Elsas et al., 1991）。描述水流诱导运输的复杂模型在几项关键研究中有所描述（Beven and Germann, 1982，Hagedorn et al., 2000，Ma et al., 2010），在此不再进一步讨论。对于本次综述，简要说明土壤质地类型、不同粘土类型的存在和土壤条件（pH 值、存在的离子类型、温度）是吸附/解吸过程的关键决定因素，这影响了移动的细菌群体在土壤中迁移的程度。在自然界中，降雨和灌溉通过土壤提供水流，尽管不规则；水流运输的程度由模型设定的规则驱动。

Wind blowing over a relatively dry soil surface also constitutes a driver of microbial translocation over distances that may be in the kilometer range (Kellogg and Griffin, 2006). Microbial cells attached to particular soil dusts (which are lifted high by the wind) can disperse over distances that reach up to 5,000 km (Kellogg and Griffin, 2006), with particles uplifts to 8,000 m (Meloni et al., 2007). Thus, only those bacteria that are able to survive under the harsh atmospheric conditions (due to UV radiation, desiccation and freezing) have been found to be detectable at sites where such dust settled (Kellogg and Griffin, 2006, Peter et al., 2014). Spore-forming bacteria (such as Bacillus species) stood out as the key organisms that are able to survive such long-distance dispersal by wind (Prospero et al., 2005). Clearly, the success of long-distance dispersal depends on the successful establishment of the incoming population in the recipient environment. As such, it depends on local soil conditions, such as water content, pH, temperature and the invader-suppressive nature of the resident community (Meola et al., 2015).
风吹过相对干燥的土壤表面也构成了微生物跨距离迁移的驱动因素，距离可能达到公里范围内(Kellogg and Griffin, 2006)。附着在特定土壤尘埃上的微生物细胞（被风高高扬起）可以传播到达 5,000 公里的距离(Kellogg and Griffin, 2006)，颗粒上升到 8,000 米(Meloni et al., 2007)。因此，只有那些能够在严酷的大气条件下（由于紫外线辐射、干燥和冻结）生存的细菌才能在这些尘埃沉降的地方被检测到(Kellogg and Griffin, 2006, Peter et al., 2014)。形成孢子的细菌（如Bacillus物种）被认为是能够通过风进行长距离传播的关键生物(Prospero et al., 2005)。显然，远距离传播的成功取决于进入种群在接收环境中的成功建立。因此，它取决于当地的土壤条件，如水分含量、pH 值、温度以及常驻群体的抑制入侵者的特性(Meola 等人，2015)。

3.3. Soil organisms mediating movement

In the light of the fact that, generally, a top soil is in water-unsaturated condition (denoted as “field capacity”), bacterial movement over longer distances will be critically dependent on the chances bacteria have to cross air gaps between soil microhabitats. A key role for “vector” organisms is thus envisioned. Hence, the movement of bacterial cells in soil is to some extent driven externally, i.e. bacterial cells can “hitchhike” along with other (moving or growing) soil organisms. This hitchhiking effect constitutes a mechanism that has been relatively understudied. For example, earthworms, nematodes, protozoa, soil fungi and even plant roots constitute major vectors that promote the dispersal of their associated bacterial cells. They may act either as “trucks” (earthworms, nematodes, protozoa) or as “networks” (fungi, plant roots). Hereunder, we examine the mechanisms behind, and potential impact of, these two modes of bacterial translocation.
鉴于一般情况下，表土处于不饱和状态（称为“田间持水量”），细菌在较长距离上的移动将严重依赖于细菌穿越土壤之间空气间隙的机会微生境。因此，“载体”生物的关键作用被设想。因此，细菌在土壤中的移动在某种程度上是由外部驱动的，即细菌可以“搭便车”与其他（移动或生长的）土壤生物一起移动。这种搭便车效应构成了一种相对未被充分研究的机制。例如，蚯蚓、线虫、原生动物、土壤真菌甚至植物根系构成了促进其相关细菌细胞扩散的主要载体。它们可以充当“卡车”（蚯蚓、线虫、原生动物）或“网络”（真菌、植物根系）。在下文中，我们将探讨这两种细菌转移模式背后的机制及其潜在影响。

3.3.1. “Trucks”

Nematodes, earthworms, protozoa, next to other soil animals (encompassing many soil arthropods), can be regarded as “trucks” that move through the soil, i.e. these organisms constitute individual transport units that can take on “bacterial cargo”. Either pulsed or gradual shedding of the bacterial cell cargo, followed by bacterial cell establishment, will lead to a particular defined dispersal trajectory of the cargo along the “truck” path. Bacterial cells may hitchhike along with such vector organisms by adhering to the available surfaces, being external (skin) or internal (e.g. intestines) (Hekman et al., 1995, Daane et al., 1996). Previous studies have shown that nematode and earthworm intestines represent complex microbial systems that enable cargo loading followed by casting-related bacterial spread through soil. Earthworms (Lumbricus terrestris, L. rubellus and Aporrhectodia trapezoides) indeed enhanced the movement of Pseudomonas fluorescens C5t (pJP4) through soil. The bacterial cell population, of 10⁸ CFU/g soil at day 0, decreased to 10^6.72 CFU/g soil at day 14 in top soil, and was not detected in deeper soil in the absence of earthworms (Daane et al., 1996). On the other hand, the presence of the earthworms moved bacteria to deeper soil parts, in dependency of the depth the earthworm could reach (up to 40 cm depth for L. terrestris). The bacterial cell density decreased with increasing soil depth (10^6.51 CFU/g soil in the top soil and 10^2.96 CFU/g soil in 35–40 cm soil, in the presence of L. terrestris) (Daane et al., 1996). Earthworm guts are known to harbor microorganisms that are acquired from the soil and subsequently selected by the host (Hekman et al., 1995, Byzov et al., 2007, Singh et al., 2015). Thus, movement of earthworms through soil promotes the dispersal of bacterial types via casting (next to shedding). Three key processes, i.e. bacterial cell uptake/adherence, survival and release to establishment, determine the rate of dispersal of bacterial cells along with the moving earthworm. In a similar way, soil nematodes (Berg et al., 2016) and arthropods also contain specialized microbiomes in their guts and on their skins that are shaped by similar processes. The potato cyst nematode Caenorhabditis elegans was found to strongly select members of the Enterobacteriaceae, Burkholderiaceae, Propionibacteriaceae, Xanthomonadaceae and Pseudomonadaceae (Berg et al., 2016), whereas Microbacteriaceae, Xanthomonadaceae, Enterobacteriaceae, Chitinophagaceae were dominant in the gut of the microarthropod Folsomia candida (Agamennone et al., 2015). These findings indicated that the soil microbiome can be strongly modulated at local sites of casting and/or shedding (Thimm et al., 1998, Agamennone et al., 2015). Moreover, death of these vector organisms will incite a decomposition process with specialized bacterial cells locally increasing in abundance. Thus a hotspot for decomposer bacterial outgrowth emerges, fostering the “net” movement within the soil.
线虫、蚯蚓、原生动物以及其他土壤动物（包括许多土壤节肢动物）可以被视为在土壤中移动的“卡车”，即这些生物构成了各自的运输单位，可以携带“细菌货物”。细菌细胞的脉冲或逐步脱落随后进入土壤并定殖，会沿着“卡车”的路径形成特定的货物传播轨迹。通过附着在可用的表面上（外部如皮肤或内部如肠道）进行搭便车，这些细菌细胞可以随着这些载体生物传播 (Hekman et al., 1995, Daane et al., 1996)。先前的研究表明，线虫和蚯蚓的肠道是复杂的微生物系统，它们可以装载货物，然后通过铸造相关的细菌扩散到土壤中。蚯蚓 (Lumbricus terrestris, L. rubellus 和 Aporrhectodia trapezoides) 确实增强了 Pseudomonas fluorescens C5t (pJP4) 在土壤中的移动。细菌细胞群在第 0 天为 10⁸ CFU/g 土壤，到第 14 天在表层土壤中降至 10^6.72 CFU/g 土壤，并且在没有蚯蚓的情况下在更深的土壤中没有检测到(Daane 等，1996). 另一方面，蚯蚓的存在使细菌移动到更深的土壤部分，取决于蚯蚓能够到达的深度（L. terrestris可达 40 厘米深度）。细菌细胞密度随着土壤深度的增加而减少（表层土壤中为 10^6.51 CFU/g 土壤，在 35-40 厘米土壤中为 10^2.96 CFU/g 土壤，存在L. terrestris的情况下）(Daane 等，1996)。已知蚯蚓肠道中含有从土壤中获取并随后被宿主选择的微生物(Hekman 等，1995, Byzov 等，2007, Singh 等，2015). 因此，蚯蚓在土壤中的移动通过分泌物（其次是蜕变）促进了细菌类型的传播。三个关键过程，即细菌细胞的摄取/附着、生存和释放到定殖，决定了随着移动的蚯蚓细菌细胞的传播速度。同样，土壤线虫 (Berg et al., 2016) 和节肢动物也在其肠道和皮肤上含有由类似过程形成的专门的微生物群落。马铃薯胞囊线虫 秀丽隐杆线虫被发现会强烈选择肠杆菌科、伯克氏菌科、丙酸杆菌科、黄单胞菌科和假单胞菌科 (Berg et al., 2016), 而 微杆菌科, 黄单胞菌科, 肠杆菌科, 几丁质单胞菌科 在微节肢动物白蚁的肠道中占主导地位 (Agamennone 等, 2015)。这些发现表明，土壤微生物群可以在铸造和/或脱落的局部位置被强烈调节 (Thimm 等, 1998, Agamennone 等, 2015)。此外，这些媒介生物的死亡将引发分解过程，专门的细菌细胞在局部增加。因此，一个分解细菌生长的热点出现，促进了土壤中的“净”运动。

3.3.2. Networks

Plant roots and fungal hyphae both form network structures consisting of interconnected biological surfaces in soil. Such interconnected surfaces, although often ephemeral, can be colonized by particular bacteria (as well as other microbes) and constitute “highways” along which bacterial cells may be able to move.
植物根系和真菌菌丝都在土壤中形成由相互连接的生物表面组成的网络结构。尽管这些相互连接的表面通常是短暂的，但可以被特定的细菌（以及其他微生物）定殖，并构成细菌细胞可能能够移动的“高速公路”。

Plant root networks – a hallmark study on the effects of plant roots showed that, mediated by type I and type III fimbriae, Klebsiella strains can effectively attach to root cap cells and to the root elongation zone of Poa pratensis, thus migrating along with growing roots (Haahtela et al., 1986). The presence of the inoculant Klebsiella on the roots stimulated root growth and branching, and hence some degree of mutualism was noticed. Similarly, Kamilova and colleagues showed that several bacteria, including Pseudomonas fluorescens, Pseudomonas putida, Aeromonas hydrophila and Pantoea agglomerans, in association with tomato roots, can act as biocontrol agents, taking profit of the extension of the roots to migrate. All bacteria were motile, showing higher colonization ability of the root than the model tomato root tip colonizer Pseudomonas fluorescens WCS365 (Kamilova et al., 2005). In a very recent study, Rhizobium radiobacter F4 was found to first colonize the primary roots (1 cm in length) of barley at 5 days post-inoculation (5 dpi), after which it spreads to the secondary roots and covers the primary and secondary roots subsequently at 30 dpi (Glaeser et al., 2016). The ability to attach to the plant root may have been the key factor that determined the successful bacterial colonization of the root. In particular, the ability to hold on to the root tips, thus, migration along with developing roots, was primordial. In contrast, flagellar dispersion and/or chemotaxis are likely crucial for microbial transport processes on mature roots, where tissues are immobile (Dupuy and Silk, 2016).
植物根系网络 – 一项关于植物根系影响的标志性研究表明，通过 I 型和 III 型菌毛介导，克雷伯氏菌菌株可以有效地附着在根冠细胞和草地早熟禾的根伸长区，从而随着根的生长迁移（Haahtela 等，1986）。接种剂克雷伯氏菌在根部的存在刺激了根的生长和分枝，因此注意到某种程度的互利共生。同样，Kamilova 和同事们表明，包括荧光假单胞菌、恶臭假单胞菌、嗜水气单胞菌和聚集泛菌在内的几种细菌与番茄根系结合，可以作为生物防治剂，利用根系的延伸进行迁移。所有细菌都是可移动的，显示出比模型番茄根尖定殖者荧光假单胞菌WCS365（Kamilova 等，2005）更高的根系定殖能力。在一项最新的研究中，根瘤菌F4 在接种后 5 天（5 dpi）首先定殖在大麦的初生根（1 厘米长）上，然后扩散到次生根，并在 30 dpi 时覆盖初生和次生根（Glaeser 等，2016）。附着在植物根部的能力可能是决定根部成功细菌定殖的关键因素。特别是抓住根尖的能力，因此，随着根的发育而迁移，是最重要的。相比之下，鞭毛分散和/或趋化性可能对成熟根部的微生物运输过程至关重要，因为此时组织是静止的（Dupuy 和 Silk, 2016）。

Hyphal networks – There is an increasing body of literature highlighting fungal growth as a key mechanism promoting bacterial movement through soil (Kohlmeier et al., 2005, Warmink and van Elsas, 2009, Furuno et al., 2012, Worrich et al., 2016a, Yang et al., 2016). Kohlmeier et al. first clearly highlighted the importance of a “fungal highway” as a transport network for particular bacteria through soil (Kohlmeier et al., 2005). This revealing finding actually was a reconfirmation of much earlier findings on fungi spurring the movement of bacteria through soil (Wong and Griffin, 1976). In our own studies, we found that the growing hyphae of the soil saprotroph Lyophyllum sp. strain Karsten can act as a “fungal highway” that facilitates the translocation of cells of a suite of Burkholderia (now Paraburkholderia) strains (Warmink and van Elsas, 2009, Nazir et al., 2012). One of these strains, P. terrae BS001, was shown to disperse along with several (basidiomycetous and actomycetous) fungi, which characterizes it as a broad-spectrum co-migrator (Warmink and van Elsas, 2009, Nazir et al., 2014). Interestingly, strain BS001 was even able to mediate the dispersion of another soil bacterium, Dyella japonica BS013 (an organism not able to migrate alone with the fungal hyphae), with Lyophyllum sp. strain Karsten (Warmink et al., 2011). A later in situ study showed that several Fusarium strains were able to facilitate the spread of Stenotrophomonas maltophilia and Ochrobactrum pectoris, 40 mm away from their original site in soil (Simon et al., 2015). Moreover, spread of particular naphthalene-degrading bacterial strains over air gaps, mediated by the soil oomycete Pythium ultimum, was also reported (Furuno et al., 2012). Importantly, the dispersal of bacterial cells along fungal hyphae improved their access to natural or anthropogenic compounds in soil, spurring the bacterial turnover of these (Banitz et al., 2016).
菌丝网络 – 越来越多的文献强调真菌生长是促进细菌通过土壤移动的关键机制 (Kohlmeier 等, 2005, Warmink 和 van Elsas, 2009, Furuno 等, 2012, Worrich 等, 2016a, Yang 等, 2016)。Kohlmeier 等首次明确强调了“真菌高速公路”作为特定细菌通过土壤的运输网络的重要性 (Kohlmeier 等, 2005)。这一揭示性发现实际上是对更早期关于真菌促进细菌通过土壤移动的发现的再次确认 (Wong 和 Griffin, 1976)。在我们自己的研究中，我们发现土壤腐生菌的生长菌丝 saprotroph Lyophyllum sp. 卡尔斯滕菌株可以充当“真菌高速公路”，促进一系列伯克氏菌（现为副伯克氏菌）菌株的细胞迁移（Warmink 和 van Elsas, 2009, Nazir 等, 2012）。其中一个菌株，P. terrae BS001，被证明能够与多种（担子菌和放线菌）真菌一起扩散，这使其成为广谱共迁移者（Warmink 和 van Elsas, 2009, Nazir 等, 2014）。有趣的是，菌株 BS001 甚至能够借助紫萁属 sp. 卡尔斯滕菌株（Warmink 等, 2011）介导另一种土壤细菌，日本独步菌 BS013（这种生物体不能单独随真菌菌丝迁移）的扩散。后来的原位研究表明，几种镰刀菌菌株能够促进嗜麦芽窄食单胞菌和黄杆菌 pectoris在土壤中从原始位置向外扩散 40 毫米(Simon et al., 2015)。此外，还报道了由土壤卵菌终极腐霉,介导的某些降解萘的细菌菌株在空气间隙中的传播(Furuno et al., 2012)。重要的是，沿着真菌菌丝的细菌细胞扩散改善了它们对土壤中天然或人为化合物的获取，从而促进了这些化合物的细菌周转(Banitz et al., 2016)。

In recent work, we found that progressively lowered soil pH restricted the survival and migration of P. terrae along fungal hyphae in soil. Remarkably, migration in the non-hyphal-extension direction was found, which showed a weak correlation with the newly-formed hyphae in this soil area (Yang et al., 2018). Very convincing evidence was found for the contention that flagella play a key role in the migration of P. terrae BS001 along with Lyophyllum sp. strain Karsten hyphae, whereas the type three secretion system (T3SS) and type four pili (T4P) had minor influences (Yang et al., 2016, Yang et al., 2017). Thus, fungal hyphae in soil forming mycelial networks promote the motility of particular bacteria, like P. terrae. We further found that only soil-dwelling hyphae, which were hydrophilic, can support bacterial migration. In contrast, aerial hyphae, which are more hydrophobic, did not allow efficient migration (Vila et al., 2016). Overall, on the basis of our findings, and in line with findings by Furuno et al. (2010), we posit that a water film formed around the soil-borne fungal hyphae is critical for the occurrence of bacterial swimming motility driven co-migration along the fungal highway.
在最近的研究中，我们发现逐渐降低的土壤 pH 值限制了P. terrae沿着土壤中真菌菌丝的生存和迁移。值得注意的是，发现了非菌丝延伸方向的迁移，这与该土壤区域中新形成的菌丝呈弱相关性(Yang et al., 2018)。有非常有说服力的证据表明，鞭毛在P. terrae BS001 与Lyophyllum sp.菌株 Karsten 菌丝的迁移中起关键作用，而三型分泌系统(T3SS)和四型菌毛(T4P)的影响较小(Yang et al., 2016, Yang et al., 2017)。因此，土壤中形成菌丝网络的真菌菌丝促进了特定细菌如P. terrae的运动。我们进一步发现，只有亲水性的土壤菌丝才能支持细菌的迁移。相比之下，更具疏水性的气生菌丝并未允许有效迁移(Vila et al., 2016)。总体而言，基于我们的研究结果，并且与Furuno et al. (2010)的发现一致，我们认为在土壤中形成的水膜对于驱动细菌游泳运动沿着真菌高速公路共同迁移的发生至关重要。

3.3.3. Processes involved in bacterial cell movement at, and colonization of, fungal hyphae in soil

Several models have been proposed for bacterial migration along with fungal networks. Based on all studies, including those of our own group, we propose the process of bacterial migration along with fungal hyphae to proceed in soil as follows:
有多种模式被提出用于解释细菌沿着真菌网络迁移的过程。基于所有研究，包括我们团队的研究，我们提出细菌沿着真菌菌丝在土壤中迁移的过程如下：

(1)
Approach: soil-borne bacterial cells get closer to an emergent or existing fungal surface, using chemotaxis-mediated short-distance movement. The approach may also be incited as a result of fungal hyphal elongation, which places the fungal surface in close vicinity of the bacterial cells. Bacterial cells may also move to fungal surfaces mediated by other soil organisms (such as other fungal hyphae, plant roots or earthworms).
接近：土壤中的细菌细胞通过趋化性短距离运动接近新生或现存的真菌表面。接近也可能由于真菌菌丝延长引起，从而使真菌表面靠近细菌细胞。细菌细胞也可能通过其他土壤生物（如其他真菌菌丝、植物根系或蚯蚓）移动到真菌表面。
(2)
Attachment: some (but not all) bacterial cells bind to the fungal surface. Key drivers are fungal nutrient-rich surface areas, such as found at the apical tip. In this step, anchoring “devices” such as T3SS and type-four pili may assist or mediate the process.
附着：一些（但不是全部）细菌细胞附着在真菌表面。关键驱动因素是真菌营养丰富的表面区域，如在顶端发现的。在此步骤中，T3SS 和四型菌毛等锚定“装置”可能会协助或介导该过程。
(3)
Growth: attached bacterial cells start to utilize nutrients secreted by the fungal hyphae and grow on the fungal surface.
生长：附着的细菌细胞开始利用真菌菌丝分泌的营养物质，并在真菌表面生长。
(4)
Spread: some (specialized) cells may spread (movement) as driven by chemotaxis. Within-population competition is a factor of importance here. Along with the bacterial density increases by growth, the locally-available nutrient levels decrease, and so competition between the cells augments. Some cells may leave the origin microsite and disperse along with the fungal hyphae. Sensing and moving towards enhanced fungal exudates (chemotaxis) may play a role. In this step, the presence of a water film around fungal hyphae is critical.
扩散：一些（专门化的）细胞可能会在趋化作用的驱动下扩散（移动）。种群内竞争在这里是一个重要因素。随着细菌密度通过生长增加，局部可用的营养水平下降，因此细胞之间的竞争加剧。一些细胞可能会离开原始微环境并沿着真菌菌丝扩散。感知和向增强的真菌分泌物（趋化作用）移动可能起到作用。在这一步中，真菌菌丝周围的水膜的存在是至关重要的。
(5)
Establishment and formation of a new niche: following the migration, the specialized bacterial cells reach new microsites at the fungal surface, establish there, and repeat the former steps 1–4.
新生态位的建立和形成：在迁移之后，专门化的细菌细胞到达真菌表面的新微位点，在那里建立并重复之前的步骤 1-4。
(6)
Biofilm formation: following cycles of steps 1–5, eventually large populations of bacterial cells occupy the hyphal surface. At enhanced cell densities, biofilms are formed around the cell populations.
生物膜形成：经过步骤 1-5 的循环后，最终大量细菌细胞占据了菌丝表面。在增强的细胞密度下，生物膜在细胞群体周围形成。
(7)
Unloading: bacterial cells are unloaded from the fungal surfaces either via dislodgement or following decay of the fungal cells. This potentially results in novel bacterial hotspots in soil, that are available for subsequent transport by any of the mechanisms/actors discussed here.
卸载：细菌细胞通过脱落或真菌细胞衰变从真菌表面卸载下来。这可能会在土壤中形成新的细菌热点，随后可以通过这里讨论的任何机制/因素进行运输。

3.3.4. Model describing bacterial dispersal through networks in soil

A model that describes the bacterial movement along with wheat plant roots was constructed by Scott et al. (Scott et al., 1995). According to the model, the movement is determined by a set of at least 22 key parameters (Table 1). These include: soil water potential, time, soil properties [diffusion coefficient of substrate in solution (D_s), impedance factor (f) that mimicks the tortuous pathway through the soil pores, soil water content (θ)], root zone characteristics [rate of exudation of substrate from root into rhizosphere (Hfx_int), rate of substrate diffusion from the rhizosphere into the bulk soil (Hfx_out), width of rhizosphere (d_r), depth of the layer (d_z), nutrient saturation constant (K_s), horizontal (A_rh) and vertical (A_rv) areas of the rhizosphere over which the diffusion of substrate will take place, volume of the rhizosphere (V_r)], next to microbial characteristics [maximum specific growth rate in dry (μ_md) and wet (μ_mw) habitat, death rate in dry (k_d) and wet (k_w) habitat, growth yield (Y)], variable parameters [bacterial concentration in dry (G_d) and wet habitat (G_w), substrate concentration in rhizosphere (S_r) and in bulk soil (S_b)]. This model matched experimental data obtained with a Pseudomonas fluorescens strain introduced into the rhizosphere of wheat fairly well (Scott et al., 1995). Thus, for P. fluorescens, movement in the rhizosphere can be depicted as a process of bacterial dispersal along extending plant roots, with key roles for movement, the utilization of nutrients and local reproduction. The length reached by the plant roots determined how far the bacterial cells can move away from the original site and the nutrient availability in the rhizosphere was critical to local bacterial cell densities that can be reached.
Scott 等人构建了一个描述细菌沿小麦植物根部运动的模型(Scott et al., 1995)。根据该模型，运动由至少 22 个关键参数决定(表 1)。这些包括：土壤水势、时间、土壤特性[溶液中底物扩散系数(D_s)、模拟通过土壤孔隙曲折路径的阻抗因子(f)、土壤水分含量（θ）]、根区特性[底物从根部分泌到根际的速度(Hfx_int)，底物从根际扩散到体积土壤的速度(Hfx_out)，根际宽度(d_r)，层深度(d_z)，营养饱和常数(K_s)，扩散底物的根际水平(A_rh)和垂直(A_rv)面积，根际体积(V_r)]，接近微生物特性[在干燥(μ_md)和湿润(μ_mw)环境下的最大特定生长速率、干燥(k_d)和湿润(k_w)环境下的死亡速率、生长产量(Y)]，变量参数[干燥条件下的细菌浓度(G_d) 和湿润栖息地 (G_w)，根际中的基质浓度 (S_r) 和大土壤中的基质浓度 (S_b)。该模型与在小麦根际中引入的 Pseudomonas fluorescens 菌株获得的实验数据相当吻合 (Scott et al., 1995)。因此，对于 P. fluorescens，在根际中的运动可以描述为沿着延伸的植物根系进行的细菌扩散过程，其中运动、营养物质的利用和局部繁殖起着关键作用。植物根系达到的长度决定了细菌细胞可以从原始位置移动多远，而根际中的营养物质可用性对可以达到的局部细菌细胞密度至关重要。

Table 1. Proposed model describing the development of plant root (rhizosphere) versus mycelium (mycosphere) associated bacterial populations (after Scott et al.¹). The model was based on the assumption that both gross translocation with extending cells and growth influence bacterial dispersal in the rhizosphere and mycosphere. Parameters that feed the model are key soil, rhizosphere/mycosphere and bacterial parameters.
表 1。提出的模型描述了植物根部（根际）与相关的菌丝体（菇圈）细菌群落的发展（根据 Scott 等人的研究。¹）该模型基于假设，即随着细胞的延伸，总运输和生长都会影响根际和菇圈中的细菌扩散。提供模型的参数是关键土壤、根际/菇圈和细菌参数。

Rhizosphere¹		Mycosphere²
Symbol	Explanation	Symbol	Explanation
Soil characteristics
D_s	Diffusion coefficient of substrate in free solution	D_s	Diffusion coefficient of substrate in free solution
f	Impedance factor that is related to the tortuous pathway through the soil pores	f	Impedance factor that is related to the tortuous pathway through the soil pores
w	Soil moisture content	w	Soil moisture content
		pH	pH of the soil³
Rhizosphere/mycosphere characteristics
Hfx_int	Rate of exudation of substrate from root into rhizosphere	Hf_int	Rate of exudation of substrate from fungal hyphae into mycosphere
Hfx_out	Rate of substrate diffusion from the rhizosphere into the bulk soil	Hfx_out	Rate of substrate diffusion from the mycosphere into the bulk soil
d_r	Width of rhizosphere	d_m	Width of mycosphere
d_z	Depth of the layer	d_z	Distance between original site and sampling site
K_s	Nutrient saturation constant	K_s	Nutrient saturation constant
A_rh	Horizontal areas of the rhizosphere over which the diffusion of substrate will take place	A_mh	Horizontal areas of the mycosphere over which the diffusion of substrate will take place
A_rv	Vertical areas of the rhizosphere over which the diffusion of substrate will take place	A_mv	Vertical areas of the mycosphere over which the diffusion of substrate will take place
V_r	Volume of the rhizosphere	V_m	Volume of the mycosphere
		θ	Fungal hyphal hydrophobicity (contact angle of hyphae)⁴
Microbial characteristics
μ_md	Maximum specific growth rate in dry habitat	μ_mw	Maximum specific growth rate in soil with moisture content at “w”⁵
μ_mw	Maximum specific growth rate in wet habitat
k_d	Death rate in dry habitat	k_dw	Death rate in soil with moisture content at “w”⁵
K_w	Death rate in wet habitat
Y	Growth yield	Y	Growth yield in soil with moisture content at “w”
Variable parameters
G_d	Bacterial concentration in dry habitat	G_w	Bacterial concentration in soil with moisture content at “w”⁶
G_w	Bacterial concentration in wet habitat
S_r	Substrate concentration in rhizosphere	S_m	Substrate concentration in mycosphere
S_b	Substrate concentration in bulk soil	S_b	Substrate concentration in bulk soil
		t	Time after bacterial inoculation⁷

1: Scott et al. (1995).
2: Proposed in this paper.
3: Low soil pH strongly restricts bacterial survival and dispersal in mycosphere (Yang et al., 2018).
4: Bacterial cells disperse along with hydrophilic fungal hyphae, not with hydrophobic hyphae (Vila et al., 2016).
5: Bacterial growth/death is associated with water availability (water activity).
6: The highest cell density that bacteria can reach might be related to soil moisture.
7: It takes longer time for bacterial cells to reach new habitats in the mycosphere with low-pH soil (Yang et al., 2018).

Given the similarity of the root and hyphal extension systems (and in the current absence of a dedicated model), we here propose that bacterial movement in the mycosphere is subjected to similar rules as given by the Scott et al model: the hyphae of saprotrophic as well as mycorrhizal fungi grow in soil by hyphal extension, to explore novel nutritive sites. Upon growth, they release small carbonaceous molecules, like glycerol and oxalate, which may serve to feed accompanying bacteria. Thus, mycosphere-adapted bacterial cells will accompany the hyphal extension in accordance with their migration and growth capacities, allowing the reaching of novel ground. To describe this, we propose the use of a modified model (Table 1) with parameters that describe the events in the mycosphere to describe the movement of bacteria along fungal hyphae. The model should be based on the concept of bacterial cell density at each specific site in the mycosphere being the result of bacterial dispersal and growth. Fungal hyphae extending over time, coupled to local nutrient levels, determine the dispersal distance of bacteria. The growth of fungal hyphae might be arrested in harsh conditions (such as in nutrient-scarce sites or at low temperatures like in winter), and may be recovered in favorable conditions. Thus, broad bacterial dispersal is subjected to the vagaries of the soil habitat and might be discontinuous. Also, properties of the mycosphere, such as its width, and its water potential (Worrich et al., 2016a) and substrate availability, are important. Finally, based on recent data (Yang et al., 2018), soil pH is a key factor to be considered in this proposed model.
鉴于根系和菌丝延伸系统的相似性（以及目前缺乏专门的模型），我们在此提出，细菌在菌根圈中的运动遵循与 Scott 等人模型相似的规则：腐生菌和菌根真菌的菌丝通过菌丝延伸在土壤中生长，以探索新的营养位点。在生长过程中，它们释放出小的碳质分子，如甘油和草酸，这些分子可能为伴随的细菌提供食物。因此，适应菌根圈的细菌细胞将根据其迁移和生长能力伴随菌丝延伸，从而到达新的区域。为了描述这一点，我们提出使用一个修改后的模型（表 1），其参数描述了菌根圈中的事件，以描述细菌沿真菌菌丝的运动。该模型应基于菌根圈中每个特定位点的细菌细胞密度是细菌扩散和生长的结果这一概念。真菌菌丝随时间延伸，结合局部营养水平，决定了细菌的扩散距离。真菌菌丝的生长可能在恶劣条件下（例如在营养稀缺的地方或像冬天那样的低温下）停止，并且在有利条件下可能恢复。因此，广泛的细菌传播受到土壤栖息地变化的影响，可能是不连续的。此外，菌圈的特性，如其宽度、水势（Worrich et al., 2016a）和基质可用性，都是重要的。最后，基于最近的数据（Yang et al., 2018），土壤 pH 值是该模型中需要考虑的关键因素。

4. An “underground transport web” that drives the migration of bacteria through soil

In line with the concept of major bacterial spread through soil by “truck-like” or “network” vector organisms, we posit that these two transport systems can lead to strongly divergent ecological outcomes. Whereas the soil trucks, particularly earthworms, protozoa and nematodes, drive pulsed cargo transport that may result in stochastic and spatially idiosyncratic delivery, the networks provided by plant roots and fungal hyphae constitute a connected “underground transport web” that facilitates, over a considerable time span, a rather continuous (and homogeneous) bacterial dispersion along the defined biological highway. Moreover, as shown in Fig. 1, plant roots, fungal hyphae and soil animals may be in contact with other transport vectors in soil, resulting in overall complex patterns of bacterial dispersal.
根据通过“卡车式”或“网络”载体生物在土壤中传播主要细菌的概念，我们认为这两种运输系统可能导致截然不同的生态结果。土壤卡车，特别是蚯蚓、原生动物和线虫，驱动脉冲货物运输，这可能导致随机和空间特异性的传递，而植物根系和真菌菌丝提供的网络构成了一个连接的“地下运输网络”，在相当长的一段时间内，沿着定义的生物高速公路促进了一种连续（且均匀）的细菌扩散。此外，如图 1所示，植物根系、真菌菌丝和土壤动物可能与土壤中的其他运输载体接触，从而导致细菌扩散的总体复杂模式。

4.1. Trucks support pulsed cargo delivery

The organisms, e.g. earthworms and/or nematodes, that constitute the “truck-like” cargo system in soil facilitate temporally- and spatially-explicit bacterial movement and delivery. Depending on their typical life modus, some specific earthworms are known to either move up/down, horizontally or erratically in soil. Upon transporting bacterial cargo, they haphazardly release cells, or do so along with casts. In their behavior in soil, they have ample opportunities to interact with plant roots or fungal hyphae, which may result in either idiosyncratic or organized patterns of bacterial dispersal (Fig. 1). For instance, one key outcome of such “truck-like” transport was found to be the movement of Sinorhizobium meliloti from bulk soil onto the roots of the legume Medicago truncatula by the soil nematode Caenorhabditis elegans. The bacterium was stably carried by the vector organism which was attracted to the plant roots (by plant-released volatiles), where the bacterial cargo was unloaded (Horiuchi et al., 2005). Additionally, earthworms utilize plant roots and fungi as food (Curry and Schmidt, 2007). Thus, the bacterial cells attached to the latter are taken up by earthworms, being converted into bacterial cargo. The earthworm L. terrestris moves vertically, from the surface to a depth exceeding 2 m (Joergensen et al., 1998), providing an extended pathway for pulsed vertical bacterial transport in soil.
生物体，例如蚯蚓和/或线虫，构成了土壤中的“卡车式”货物系统，便于细菌在时间和空间上的移动和递送。根据它们的典型生活模式，一些特定的蚯蚓被认为会向上/向下、水平或不规则地在土壤中移动。在运输细菌货物时，它们会随机释放细胞，或连同粪便一起释放。在土壤中的行为中，它们有大量机会与植物根或真菌菌丝相互作用，这可能导致细菌扩散的特定或有序模式 (图 1)。例如，这种“卡车式”运输的一个关键结果是 Sinorhizobium meliloti 从普通土壤移到豆科植物 Medicago truncatula 根部，由土壤线虫 Caenorhabditis elegans 完成的。细菌被稳定地携带在被吸引到植物根部（通过植物释放的挥发物）的载体生物中，在那里细菌货物被卸载（Horiuchi et al., 2005）。此外，蚯蚓利用植物根和真菌作为食物（Curry and Schmidt, 2007）。因此，附着在后者上的细菌细胞被蚯蚓摄取，转化为细菌货物。蚯蚓L. terrestris垂直移动，从地表到超过 2 米的深度（Joergensen et al., 1998），为土壤中脉冲垂直细菌运输提供了延长的路径。

4.2. Networks yield highways for continuous cargo delivery

In previous work, the mycosphere dweller P. terrae BS001 was translocated over 40 mm in soil, along with several fungal species, including the saprotroph Lyophyllum sp. strain Karsten, the phytopathogens Rhizoctonia solani AG3 and Fusarium oxysporum Fo47, and the biocontrol agent Trichoderma asperellum 302 (Nazir et al., 2014). Use of the Scott et al. theory allowed us to estimate the movement of strain BS001 over larger distances and time spans (using theoretical conditions of no competition, like in the laboratory experiments). The result of such simulations indicated that, given transport-favorable parameter settings, the networks that form by these fungi in soil can facilitate the spread of BS001, from tens of centimeter to meter distances over periods of months. As an example, the soil saprotroph Lyophyllum sp. strain Karsten, accompanied by P. terrae BS001, was found to extend 2.6 mm/day (resulting in 45 cm – 6 months; 1.8 m – 2 years) in soil sampled from Droevendaal (Wageningen, Netherlands; Nazir et al., 2012). Although not proven, we expect the soil fungus Armillaria ostoyae to constitute a major soil transportation network. This fungus has been described as the largest organism on Earth, being able to occupy ∼10 km² belowground as a single organism (Ferguson et al., 2003). Given the potential function of this very extensive belowground hyphal network, highly revealing experiments may be cogitated with respect to the movement of cells of bacteria that associate with it.
在之前的工作中，菌球居民P. terrae BS001 在土壤中被转移了超过 40 毫米，同时还有几种真菌物种，包括腐生菌Lyophyllum sp. Karsten 菌株，植物病原菌Rhizoctonia solani AG3 和Fusarium oxysporum Fo47，以及生物防治剂Trichoderma asperellum 302 (Nazir et al., 2014)。使用 Scott 等人的理论使我们能够估算 BS001 菌株在更大距离和时间跨度上的移动（使用无竞争的理论条件，如实验室实验中）。这种模拟的结果表明，在运输有利的参数设置下，这些真菌在土壤中形成的网络可以促进 BS001 的传播，从几十厘米到几米的距离，持续数月。例如，土壤腐生菌Lyophyllum sp. Karsten 菌株，伴随着P. terrae BS001，在从 Droevendaal（瓦赫宁根，荷兰；Nazir et al., 2012）采集的土壤中，发现其延伸速度为 2.6 毫米/天（导致 45 厘米 - 6 个月；1.8 米 - 2 年）。虽然尚未证实，但我们预计土壤真菌蜜环菌构成了一个主要的土壤运输网络。据描述，这种真菌是地球上最大的生物，能够以单个生物体的形式占据约 10 平方公里的地下空间（Ferguson et al., 2003）。鉴于这种非常广泛的地下菌丝网络的潜在功能，可能会考虑进行高度揭示性的实验，以研究与其相关的细菌细胞的运动。

On top of the fungal-driven bacterial spread through soil, connections with other fungal hyphae and/or plant roots form in a dynamic manner. For instance, common mycorrhizal networks play a critical role in long-distance transport of nutrients through the soil ecosystem (Bücking et al., 2016). Thus, a picture emerges of an often large (semi)continuous fungal-mediated connected belowground network, along which specific bacteria are able to migrate in accordance with the local factors affecting this migration. Additionally, some roots of trees reach deep soil layers (up to tens of meters), and distribute widely in top soil, facilitating vertical as well as horizontal bacterial dispersal. Thus, next to the afore-described water- and wind-driven dispersal, a complex transport web formed by earthworms, plant roots and fungal hyphae in top soil may grossly mediate bacterial dispersal (Fig. 1).
在真菌驱动的细菌通过土壤传播的基础上，与其他真菌菌丝和/或植物根系的连接以动态的方式形成。例如，普通的菌根网络在通过土壤生态系统进行长距离养分运输中起着关键作用(Bücking et al., 2016)。因此，出现了一幅通常是大型（半）连续的真菌介导的地下连接网络的图景，沿着这些网络，特定的细菌能够根据影响这种迁移的局部因素进行迁移。此外，一些树木的根系深入土壤层（深达数十米），并在表层土壤中广泛分布，促进了垂直和水平的细菌扩散。因此，除了上述的水和风驱动的扩散外，由蚯蚓、植物根系和表层土壤中的真菌菌丝形成的复杂运输网络可能大大介导细菌的扩散(图 1)。

5. Ecological and evolutionary effects of bacterial dispersal through soil

The nutrients (sources of carbon and energy) that support the survival and growth of bacteria in soil are often distributed in a very discontinuous way. Thus, in most soils, bacteria occur in nutrient-exhausted microhabitats, whereas several hotspots of enhanced nutritional status may exist only millimeters away. In these, a suite of energy-rich nutrients is – although often ephemerally – available. Such hotspots can be found in specific soil sites such as the mycosphere, the mycorrhizosphere, the rhizosphere, the drillosphere and the detritusphere (Kuzyakov and Blagodatskaya, 2015). By moving in the soil matrix, bacterial cells are able to explore newly-available soil areas and thus utilize the locally available nutrients from which they had previously been separated. Thus, next to water-driven transport, the presence of either an underground transportation network or a “truck delivery” system, or both, are key assets that greatly foster net bacterial dispersal rates in unsaturated soils.
土壤中支持细菌生存和生长的营养物质（碳和能量的来源）通常分布得非常不连续。因此，在大多数土壤中，细菌存在于营养耗尽的微生境中，而几个营养状态增强的热点可能仅存在于几毫米之外。在这些热点中，一组富含能量的营养物质虽然通常是短暂的，但仍然可用。这些热点可以在特定的土壤部位找到，例如菌圈、菌根圈、根际、钻孔圈和碎屑圈（Kuzyakov and Blagodatskaya, 2015）。通过在土壤基质中移动，细菌细胞能够探索新可用的土壤区域，从而利用之前被分隔开的局部可用营养物质。因此，除了水驱动的运输外，存在地下运输网络或“卡车运输”系统，或两者兼有，是极大促进非饱和土壤中细菌净扩散率的关键资产。

Extracellular DNA (eDNA) that enters soil as a result of cell death and lysis has also been considered to play a key role in soil. First, it can be utilized as a source of C, N and P by heterotrophic microorganisms (Levy-Booth et al., 2007). Secondly, it may have a role in biofilm formation (Pietramellara et al., 2009). Finally, it may be (horizontally) transferred into bacterial cells, spurring adaptive processes (Nielsen et al., 2007). Motile bacterial cells in soil may acquire eDNA and either use it as a nutrient source, or as a source of novel information. Conversely, they may also serve as providers of eDNA in the local bacterial communities. Thus, bacterial dispersal clearly plays a key role in bacterial community evolution in soil.
细胞死亡和裂解导致进入土壤的细胞外 DNA（eDNA）也被认为在土壤中起着关键作用。首先，它可以被异养微生物用作 C、N 和 P 的来源（Levy-Booth 等，2007）。其次，它可能在生物膜形成中起作用（Pietramellara 等，2009）。最后，它可能（水平地）转移到细菌细胞中，促进适应过程（Nielsen 等，2007）。土壤中的运动性细菌细胞可能获取 eDNA，并将其用作营养来源或新信息的来源。相反，它们也可能作为局部细菌群落中的 eDNA 提供者。因此，细菌的扩散显然在土壤中细菌群落的进化中起着关键作用。

Bacterial dispersal may be a conditio-sine-qua-non for the efficient remediation of polluted soil that needs bacterially-mediated degradation activity. An important early finding was that fungi (Kohlmeier et al., 2005, Furuno et al., 2012) and/or earthworms (Li et al., 2015) are able to mediate the movement of pollutant-degrading bacteria to key sites in soil, thus spurring the degradation of the toxic compounds. The fungal-mediated physical “highway” was posited to mediate bacterial access to the pollutants (Banitz et al., 2012, Banitz et al., 2016, Knudsen et al., 2013, Worrich et al., 2016a, Worrich et al., 2016b, Otto et al., 2017a). Presumably, this included positive chemotaxis towards the pollutants (Furuno et al., 2010), the overall outcome being fungal-mediated stimulation of bacterial survival and growth. Clearly, the mechanism enhanced the ecological opportunities for the bacteria, as described (Warmink and van Elsas, 2009, Yang et al., 2018). Here, one should take into account that also non-single-strain migrator bacteria may move along with the fungal hyphae, by a hitchhiking effect (Warmink et al., 2011). Finally, fungal mycelia were also found to facilitate predators (Bdellovibrio bacteriovorus 109J) to catch their prey bacteria Pseudomonas fluorescens LP6a (Otto et al., 2017b). This process enhanced the fitness of the predator as well as the prey, affecting ecosystem function.
细菌扩散可能是高效修复需要细菌介导降解活动的污染土壤的必要条件。一个重要的早期发现是，真菌（Kohlmeier et al., 2005，Furuno et al., 2012）和/或蚯蚓（Li et al., 2015）能够介导污染物降解细菌向土壤关键部位的移动，从而促进有毒化合物的降解。真菌介导的物理“高速公路”被认为可以介导细菌接触污染物（Banitz et al., 2012，Banitz et al., 2016，Knudsen et al., 2013，Worrich et al., 2016a，Worrich et al., 2016b，Otto et al., 2017a）。据推测，这包括对污染物的正趋化性 (Furuno et al., 2010)，总体结果是由真菌介导的细菌存活和生长的刺激。显然，这一机制增强了细菌的生态机会，如所述(Warmink and van Elsas, 2009, Yang et al., 2018)。在这里，还应考虑到非单菌株迁移细菌也可能通过搭便车效应沿着真菌菌丝移动(Warmink et al., 2011)。最后，真菌菌丝体也被发现可以促进捕食者(Bdellovibrio bacteriovorus 109J)捕捉其猎物细菌Pseudomonas fluorescens LP6a (Otto et al., 2017b)。这一过程增强了捕食者和猎物的适应性，影响了生态系统功能。

On another notice, some phytopathogens (Leben, 1984) or human pathogens (Williams et al., 2006) were found to disperse in soil, thus reaching vegetable crops, which is an undesirable process that may threaten plant and human health. One solution to control such pathogens may be the use of highly mobile antagonistic bacteria, that can efficiently translocate along vector organisms, and thus chase and reach the pathogens to exert antagonistic effects.
另一个通知，一些植物病原体（Leben, 1984）或人类病原体（Williams et al., 2006）被发现可以在土壤中传播，从而到达蔬菜作物，这是一个可能威胁植物和人类健康的不良过程。控制此类病原体的一种解决方案可能是使用高度移动的拮抗细菌，这些细菌可以沿着载体生物高效转移，从而追踪并到达病原体以发挥拮抗作用。

With respect to ecological effects, some fungal-associated bacteria can exert beneficial effects to the host. For instance, P. terrae BS001 was found to protect its fungal host, Lyophyllum sp. strain Karsten, against the antifungal agent cycloheximide present in the soil (Nazir et al., 2014). Similarly, the hypermotile P. fluorescens F113 strain showed higher competitive colonization ability on alfalfa root surfaces than other strains, thus replacing other strains at the root surface. This improved biocontrol activity (Barahona et al., 2011). Moreover, other plant growth promoting rhizobacteria, such as bacteria belonging to the genera Burkholderia and Pseudomonas, can enhance plant growth (Pii et al., 2015) and undefined gut-associated bacteria have been reported to provide essential amino acids for earthworms (Larsen et al., 2016). Dispersal extends the living area of these bacteria, and enhances the beneficial effects exerted on their hosts. Thus, the interactions between bacterial cells and their hosts can be regarded as mutualistic if dispersal facilitation is included in our considerations.
关于生态效应，一些与真菌相关的细菌可以对宿主产生有益的影响。例如，P. terrae BS001 被发现可以保护其真菌宿主，Lyophyllum sp. Karsten 菌株免受土壤中存在的抗真菌剂放线菌酮的侵害 (Nazir 等, 2014)。同样，超运动型P. fluorescens F113 菌株在苜蓿根表面表现出比其他菌株更高的竞争性定殖能力，从而取代了根表面的其他菌株。这提高了生物防治活性 (Barahona 等, 2011)。此外，其他植物生长促进根际细菌，如属于Burkholderia 和Pseudomonas 属的细菌，可以促进植物生长 (Pii 等, 2015) 和未定义的肠道相关细菌已被报道为蚯蚓提供必需氨基酸（Larsen et al., 2016）。扩散延伸了这些细菌的生活区域，并增强了对其宿主的有益作用。因此，如果在我们的考虑中包括扩散促进作用，细菌细胞与其宿主之间的相互作用可以被视为互利共生。

6. Conclusions

Bacterial dispersal through soil occurs in diverse ways and is affected by several environmental factors. A key emerging concept is that of an underground transport network, in which both (temporally-restricted) continuous transport (plant root and fungal networks) and pulsed transport (“truck-like” agents) are taking place. Dispersal is key to applications in environmental management, such as in polluted soil. Use of bacterial-dispersal-enhancing soil organisms, combined with pollutant-degrading bacteria, may improve in situ degradation efficiencies. Also, the use of combined biological agents can facilitate bacterial cells in colonizing plant roots and exert plant-beneficial effects on these. Additionally, bacterial dispersal agents may play an important role in the spread of phytopathogens between plant roots. Thus, it is critical to avoid dispersal of the latter organisms via these avenues, along with enhanced combatting of these. Moreover, human pathogens can be carried by similar migration avenues through the soil. In cases of massive transport, this may enhance the incidence of disease incited from edible crops. Thus, bacterial dispersal in soil is an important environmental issue. In specific cases, the diverse modes of translocation should be scrutinized in order to assess the chances of success of application (bioremediation) or the risks associated with pathogens. Finally, this paper has focused on the dispersal of bacteria, where we know that Archaea do occur in considerable numbers in soil, and have key specialized roles (for instance, in ammonia oxidation and methane formation) in there. Moreover, motility in Archaea has been reported widely (Kinosita et al., 2016, Legerme et al., 2016, Albers and Jarrell, 2018). Thus, we here argue that – although data are scarce – it is likely that also archaeal cells disperse along with vector organisms and extend their range of ecological action to microhabitats away from their original sites in soil.
细菌通过土壤的扩散方式多种多样，并受到多种环境因素的影响。一个新兴的重要概念是地下运输网络，其中既有（时间上受限的）连续运输（植物根和真菌网络），也有脉冲运输（“卡车”载体）。扩散对环境管理的应用至关重要，比如在污染土壤中。使用促进细菌扩散的土壤生物，结合降解污染物的细菌，可以提高原位降解效率。此外，使用联合的生物载体可以帮助细菌细胞在植物根部定殖，并对其产生有益的植物效应。此外，细菌扩散载体可能在植物根部之间传播植物病原体方面发挥重要作用。因此，必须避免通过这些途径扩散后者生物，同时强化对它们的防治。此外，人类病原体也可能通过类似的迁移途径在土壤中传播。在大量运输的情况下，这可能增加可食用作物引发疾病的发生率。因此，土壤中的细菌扩散是一个重要的环境问题。在特定情况下，应仔细审查不同的转移方式，以评估应用（生物修复）的成功机会或与病原体相关的风险。最后，本文重点讨论了细菌的扩散，我们知道古菌在土壤中也以相当数量存在，并在其中发挥关键的专业作用（例如，在氨氧化和甲烷形成中）。此外，古菌的运动能力已被广泛报道（Kinosita et al., 2016，Legerme et al., 2016，Albers and Jarrell, 2018）。因此，我们在此认为——尽管数据稀少——古菌细胞也可能与载体生物一起扩散，并将其生态作用范围扩展到远离其原始土壤位置的微生境。

7. Declarations of interest

None.

Acknowledgments

The authors thank Francisco Dini Andreote for reading and commenting on the paper. Pu Yang was financially supported by the China Scholarship Council (CSC), as well as the Soil Biotechnology Foundation (Groningen).

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Irrigation Method Matters: Contamination and Die-off Rates of Escherichia coli on Dry Bulb Onions After Overhead and Drip Irrigation in Washington State (2022–2023)
2024, Journal of Food Protection
Two U.S. outbreaks of salmonellosis in 2020 and 2021 were epidemiologically linked to red onions. The 2020 outbreak investigation implicated the production of agricultural water as a likely contamination source. Field trials were designed to investigate the prevalence and survival of Escherichia coli (surrogate for Salmonella) on dry bulb onions after the application of contaminated irrigation water at the end of the growing period. Irrigation water was inoculated at 3 log most probable number (MPN)/100 mL (2022 and 2023) or 5 log MPN/100 mL (2023, drip only) with a cocktail of rifampin-resistant E. coli and applied with the final irrigation (0.4 acre-inch/0.4 ha-cm) to onions. Onion bulbs (40 or 80) were sampled immediately after irrigation and throughout field curing (4 weeks) and E. coli was enumerated using an MPN method. For drip irrigation, at 3 log MPN/100 mL E. coli was detected on 13% of onions at 24 h but not detected at 0 h; at 5 log MPN/100 mL for drip irrigation applied to saturated soil, E. coli was detected in 63% of onions at 0 h. Prevalence significantly (P < 0.05), decreased after 7 d of curing with cell densities of 1–1,400 MPN/onion. At the end of field curing in 2023, 1/80 of onions had detectable E. coli (2.04 MPN/onion). E. coli was detected in a significantly smaller percentage of onions (2022: 13%; 2023: 68%) after a contaminated drip irrigation event compared to overhead irrigation (98–100%; P < 0.05). After overhead irrigation, E. coli was detected in onions (1–1,000 MPN/onion) on day 0. Prevalence decreased significantly (P < 0.05) after 7 d of field curing in both years (2022: 15%; 2023: 7%). E. coli was not detected on Calibra onions (80/year) at the end of field curing in either year but was detected at <12 MPN/onion in 2.5–3.75% of onions (n = 80) for other cultivars. These data confirm limited contamination risk associated with drip irrigation water quality and begin to quantify contamination risks associated with overhead irrigation of dry bulb onions.
Biochar effects on salt-affected soil properties and plant productivity: A global meta-analysis
2024, Journal of Environmental Management
Biochar has been recognized as a promising practice for ameliorating degraded soils, yet the consensus on its effects remains largely unknown due to the variability among biochar, soil and plant. This study therefore presents a meta-analysis synthesizing 92 publications containing 987 paired data to scrutinize biochar effects on salt-affected soil properties and plant productivity. Additionally, a random meta-forest approach was employed to identify the key factors of biochar on salt-affected soil and plant productivity. Results showed that biochar led to significant reductions in electrical conductivity (EC), bulk density (BD) and pH by 7.4%, 4.7% and 1.2% compared to the unamended soil, respectively. Soil organic carbon (by 55.1%) and total nitrogen (by 31.3%) increased significantly with biochar addition. Moreover, biochar overall enhanced plant productivity by 31.5%, and more pronounced increases in forage/medicinal with higher salt tolerance than others. The results also identified that the soil salinity and biochar application rate were the most important co-regulators for EC and PP changes. The structural equation model further showed that soil salinity (P < 0.001), biochar pH (P < 0.001) and biochar specific surface area (P < 0.01) had a significant negative effect on soil EC, but it was positively impacted by biochar pyrolysis temperature (P < 0.05). Furthermore, plant productivity was positively affected by biochar pH (P < 0.001) and biochar feedstock (P < 0.01), while negatively influenced by biochar pyrolysis temperature (P < 0.01). This study highlights that woody biochar with 7.6 < pH < 9.0 and pyrolyzed at 400–600 °C under 30–70 t ha⁻¹ application rate in moderately saline coarse soils is a recommendable pattern to enhance forage/medicinal productivity while reducing soil salinity. In conclusion, biochar offers promising avenues for ameliorating degradable soils, but it is imperative to explore largescale applications and field performance across different biochar, soil, and plant types.
Effects of conventional, organic and conservation agriculture on soil physical properties, root growth and microbial habitats in a long-term field experiment
2024, Geoderma
Soil structure is important for plant growth and ecosystem functioning, and provides habitat for a wide range of soil biota. So far, very few studies directly compared the effects of three main farming practices (conventional, organic and conservation agriculture) on soil structure and soil physical properties. Here, we collected undisturbed soil cores from the FArming System and Tillage long-term field experiment (FAST) near Zurich (Switzerland). This trial compares the effects of conventional tillage, conventional no-tillage, organic tillage and non-inversion reduced tillage under organic farming since 2009. We assessed 28 soil chemical and physical properties and related them to root and microbial biomass as well as to the diversity of bacteria and fungi. Tillage decreased bulk density (−14 %) and penetration resistance (−40 %) compared to no/reduce-tillage, potentially promoting a facilitative environment for plant root growth. Water holding capacity varied among systems, being the lowest in conventional tillage and highest (+10 %) in organic reduced tillage. We observed that microbial biomass and rhizosphere microbial diversity was positively associated with water holding capacity and the occurrence of mesopores. The presence of mesopores could provide additional niche space for microbes possibly explaining its positive effect on microbial diversity. Soil microbial biomass and rhizosphere microbial diversity were higher in plots subjected to soil conservation practices, indicating that tillage has a detrimental effect on soil microbes. Our work demonstrates that organic, conventional and conservation agriculture create contrasting soil physical environments. This work highlights the trade-off between creating a facilitative environment for root growth by tillage and maintaining complex and diverse soil microhabitats for microbes under conservation agriculture.
Long-term cover crop monocultures and mixtures improve soil multifunctionality and shift microbial communities and functions
2024, European Journal of Agronomy
Long-term cover crops are an emerging approach for achieving sustainable agriculture by reducing fertilizer use and enhancing soil quality. However, soil microbial communities, multifunctionality (i.e., the ability of soil ecosystems to simultaneously provide and maintain multiple ecological functions), and their relationships in cover crops remain poorly understood, especially in cover crop mixtures. To address these issues, here, we conducted a 15-year field experiment under different cover crop deployments (one legume and one brassica grown in monoculture or in mixture) in Carya cathayensis plantations. We found that cover crops significantly increased soil microbial diversity and multifunctionality, especially in mixtures. The bacterial and fungal compositions was significantly affected by cover crops. Interestingly, some taxa may serve as potential indicator species for nutrient status (i.e., bacterial Subgroup_2, Subgroup_6 and Subgroup_17). Cover crops significantly increased beneficial microbial functions (e.g., nitrogen fixation) but decreased pathogen-related functions (e.g., pathotroph). Bacterial and fungal community assemblages under cover crops were dominated by stochastic processes. Cover crops, especially mixtures, had a higher habitat niche breadth (Bcom). In addition, cover crops have more complex and stable bacterial and fungal networks. Partial least squares path modeling further confirmed that the variations in soil multifunctionality were largely related to nutrient resources. Importantly, the relative abundance of rare microbial taxa was also highly correlated with soil multifunctionality. Overall, our study illustrates that the use of cover crops in the long term can foster soil microbial specific taxa and contribute to improved soil multifunctionality. Our study provides support for the benefits of a legume-brassica mixture over monocultures of either and a theoretical basis for exploring cover crops as an ecological management model.
Biochar as a sustainable tool for improving the health of salt-affected soils
2023, Soil and Environmental Health
Salt-affected soil has become one of the major threats to soil health. However, the evaluation of biochar amendment effects and the underlying mechanisms on the physical, chemical, and biological indicators used for assessing the health of salt-affected soils is lacking. This review summarized biochar performance and mechanisms in improving the health of salt-affected soils. Biochar addition significantly improved soil physico-chemical properties by enhancing aggregate stability (15.0–34.9%), porosity (8.9%), and water retention capacity (7.8–18.2%), increasing cation exchange capacity (21.1%), soil organic carbon (63.1%), and nutrient availability (31.3–39.9%), as well as decreasing bulk density (6.0%) and alleviating salt stress (4.1–40.0%). Following biochar incorporation, soil biological health can also be improved, particularly enhancing microbial biomass (7.1–25.8%), facilitating enzyme activity (20.2–68.9%), and ultimately increasing plant growth. To properly assess the health of salt-affected soils, it is important to select indicators related to ecological service functions including plant production, water quality, climate change, and human health. This will improve the evaluation of soil multifunctionality and enhance current soil health assessment methods. Finally, limitations and future needs of biochar research and biochar-based technologies for soil health assessment in salt-affected soils are discussed. Based on a global meta-analysis to illustrate biochar effects on salt-affected soil health indicators, this review offers valuable insights for developing sustainable biochar-based tools for remediating salt-affected soil.
Enhancement on migration and biodegradation of Diaphorobacter sp. LW2 mediated by Pythium ultimum in soil with different particle sizes
2024, Frontiers in Microbiology
The composition and structure of natural soil are very complex, leading to the difficult contact between hydrophobic organic compounds and degrading-bacteria in contaminated soil, making pollutants hard to be removed from the soil. Several researches have reported the bacterial migration in unsaturated soil mediated by fungal hyphae, but bacterial movement in soil of different particle sizes or in heterogeneous soil was unclear. The remediation of contaminated soil enhanced by hyphae still needs further research.
In this case, the migration and biodegradation of Diaphorobacter sp. LW2 in soil was investigated in presence of Pythium ultimum.
Hyphae could promote the growth and migration of LW2 in culture medium. It was also confirmed that LW2 was able to migrate in the growth direction and against the growth direction along hyphae. Mediated by hyphae, motile strain LW2 translocated over 3 cm in soil with different particle size (CS1, 1.0–2.0 mm; CS2, 0.5–1.0mm; MS, 0.25–0.5 mm and FS, <0.25 mm), and it need shorter time in bigger particle soils. In inhomogeneous soil, hyphae participated in the distribution of introduced bacteria, and the total number of bacteria increased. Pythium ultimum enhanced the migration and survival of LW2 in soil, improving the bioremediation of polluted soil.
The results of this study indicate that the mobilization of degrading bacteria mediated by Pythium ultimum in soil has great potential for application in bioremediation of contaminated soil.

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Outline

Cited by (85)

Figures (1)

Tables (1)

Applied Soil Ecology

Highlights

Abstract

Keywords

1. Introduction – The importance of bacterial dispersal for differentiation processes and soil functioning

2. Bacterial dispersal is affected by the soil pore network and water properties

3. Bacterial movement through soil

3.1. Active movement

3.2. Passive movement

3.3. Soil organisms mediating movement

3.3.1. “Trucks”

3.3.2. Networks

3.3.3. Processes involved in bacterial cell movement at, and colonization of, fungal hyphae in soil

3.3.4. Model describing bacterial dispersal through networks in soil

4. An “underground transport web” that drives the migration of bacteria through soil

4.1. Trucks support pulsed cargo delivery

4.2. Networks yield highways for continuous cargo delivery

5. Ecological and evolutionary effects of bacterial dispersal through soil

6. Conclusions

7. Declarations of interest

Acknowledgments

References

Cited by (85)

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Effects of conventional, organic and conservation agriculture on soil physical properties, root growth and microbial habitats in a long-term field experiment

Long-term cover crop monocultures and mixtures improve soil multifunctionality and shift microbial communities and functions

Biochar as a sustainable tool for improving the health of salt-affected soils

Enhancement on migration and biodegradation of Diaphorobacter sp. LW2 mediated by Pythium ultimum in soil with different particle sizes

Review 评论Mechanisms and ecological implications of the movement of bacteria in soil土壤中细菌运动的机制及生态意义

Highlights

Abstract

Keywords

1. Introduction – The importance of bacterial dispersal for differentiation processes and soil functioning

2. Bacterial dispersal is affected by the soil pore network and water properties

3. Bacterial movement through soil

3.1. Active movement

3.2. Passive movement

3.3. Soil organisms mediating movement

3.3.1. “Trucks”

3.3.2. Networks

3.3.3. Processes involved in bacterial cell movement at, and colonization of, fungal hyphae in soil

3.3.4. Model describing bacterial dispersal through networks in soil

4. An “underground transport web” that drives the migration of bacteria through soil

4.1. Trucks support pulsed cargo delivery

4.2. Networks yield highways for continuous cargo delivery

5. Ecological and evolutionary effects of bacterial dispersal through soil

6. Conclusions

7. Declarations of interest

Acknowledgments

References

Review 评论
Mechanisms and ecological implications of the movement of bacteria in soil
土壤中细菌运动的机制及生态意义