Selective successional transport of bacterial populations from rooted agricultural topsoil to deeper layers upon extreme precipitation events

Highlights

• Maize rhizosphere bacteria are selectively transported with seepage water.

• A high dynamics of microbial populations mobilized during seepage events was observed.

• Seepage water acts as a conduit for microbes and substrates between surface and subsoils.

Abstract

Substantial amounts of organic matter are mobilized from upper soil layers during extreme precipitation events. This results in considerable fluxes of carbon from plant-associated topsoil to deeper mineral soil and to groundwater. Microbes constitute an important part of this mobile organic matter (MOM) pool. Previous work has shown that specific bacteria associated with the rhizosphere of decaying maize roots were selectively transported with seepage water upon snowmelt in winter. However, effective mechanisms of mobilization and also possible distinctions to microbial transport for living root systems remain poorly understood. In the present study, bacteria in seepage water were sampled from lysimeters at an experimental maize field after extreme rain events in summer. We show that a distinctive subset of rhizoplane-associated bacterial populations was mobilized after summer rain, especially including abundant members of the Bacteroidetes, representing a microbial conduit for fresh plant-derived carbon inputs into deeper soil layers. Marked distinctions of seepage communities were not observed between lysimeters with a different relative contribution of preferential vs. matrix flow. Time-resolved analyses of seepage water during an artificial rain event revealed temporal patterns in the mobilization of certain lineages, with members of the Chitinophagaceae, Sphingomonadaceae, and Bradyrhizobiaceae preferentially mobilized in early and late seepage fractions, and members of the candidate phyla Parcubacteria and Microgenomates mobilized mostly in intermediate fractions. While average bacterial cell counts were at ∼10⁷ ml⁻¹ in seepage water, the recovery of amended fluorescently labeled cells of Arthrobacter globiformis was low (0.2–0.6%) over seepage events. Still, mobilized bacteria clearly have the potential to influence bacterial activities and communities in subsoils. These findings demonstrate that dynamic hydraulic events must be considered for a better understanding of the connectivities between microbial populations and communities in soil, as well as of the links between distinct carbon pools over depth.

Introduction

Soil is the largest terrestrial reservoir of organic carbon, playing an essential role in global carbon sequestration (Lal, 2004). A primary source of soil organic matter (SOM) is provided by plants (Kögel-Knabner, 2002), which largely determine the distribution of OM (Jobbágy and Jackson, 2000). Transport of OM from topsoil to deeper soil layers with seepage water is a main component of carbon fluxes in soil, representing a significant share of fresh inputs of OM to subsoil and even to groundwater (Rumpel and Kögel-Knabner, 2011; Küsel et al., 2016).

Mobile organic matter in soil consists mostly of dissolved and colloidal organic carbon, including biocolloids like bacteria, fungi and their fragments (Totsche et al., 2007; Lehmann et al., 2018). The mechanisms of release and transport of such biocolloids and larger organic particles from the topsoil to subsoil are complex and poorly understood so far. They are highly influenced by dynamic environmental conditions like fluctuations in soil moisture, soil gas and temperature (Or et al., 2007). The soil pore network structure is a main controlling factor as a path for these fluxes, especially with the presence of macro- and biopores favoring the preferential and pronounced transport of OM (Jacobsen et al., 1997; Lægdsmand et al., 1999) and microorganisms (Bundt et al., 2001; Wang et al., 2013; Dibbern et al., 2014). The mobilization of viable microbes from topsoil mediated by preferential flow could also act as an important influx of biodiversity to subsoils, where the translocated microbes may significantly contribute to local microbial activities (Kieft et al., 1998; Jaesche et al., 2006; Küsel et al., 2016).

The importance of understanding bacterial mobility and transport mechanisms in soil has been increasingly recognized, mostly connected to the input of potential pathogens to groundwater (Bradford et al., 2013). In soil, bacteria either move actively (Sen, 2011), or are mobilized passively by advection after release to the mobile water phase (Wang et al., 2013), via nematodes (Knox et al., 2004), or along growing plant roots (Feeney et al., 2006) and fungal hyphae (Simon et al., 2015). Substantial amounts of suspended materials including bacterial biomass can be transported vertically from topsoil (Totsche et al., 2007; Lehmann et al., 2018), especially triggered by weather events producing large amounts of seepage, such as snowmelt or strong precipitation (Dibbern et al., 2014). Numerous column studies have been conducted to address how the transport of pathogenic bacteria amended to soil is affected by various physical, chemical and biological factors (Bradford et al., 2013). Distinct features, such as cellular shape (Weiss et al., 1995), hydrophobicity (Kim et al., 2009), surface charge (Bolster et al., 2009), and bacterial interactions (Stumpp et al., 2011) were found to influence bacterial detachment and transport behavior. However, while central aspects of the transport of selected bacterial strains in soil have been intensively investigated, our understanding of the release and transport of complex indigenous microbiota in natural soils remains limited.

We have previously addressed this knowledge gap by characterizing natural bacterial communities mobilized with seepage water after snowmelt in late winter on an experimental maize field in Germany (Dibbern et al., 2014). The findings suggested that preferential flow along root channels played an important role in the transport of topsoil bacteria to deeper soil layers, and specific subsets of bacteria associated with decaying roots were selectively mobilized. However, these first insights did not address the potential impacts of more pronounced precipitation events and variability of soil moisture on living root systems in summer. In the present study, we hypothesize that (i) distinct subsets of root-associated bacterial populations will be selectively mobilized and transported to deeper soil layers along living root channels in summer; and (ii) a differential contribution of effective flow paths, i.e. preferential vs. matrix flow, during seepage events should be reflected in dynamics of transported microbiota. To address this, we conducted seepage water sampling after natural and artificial extreme rain events in late summer. Via direct time-resolved sampling, we characterized mobile organic matter (MOM), related physicochemical parameters as well as mobilized complex microbiota throughout the seepage process and compared them to the surrounding soil- and root-associated microbiomes. Furthermore, we used fluorescently labeled viable cells of a bacterial strain characteristic of the site as a tracer, to quantify their mobilization and transport behavior during seepage events.