Hitchhikers on the fungal highway: The helper effect for bacterial migration via fungal hyphae
Research highlights
► We addressed the basis of the community migration on fungal hyphae. ► The migration helper effect exerted by particular migrators on the community was studied. ► We used, as a model, the migration-proficient Burkholderia terrae BS001 as helper strain. ► Dyella japonica BS003, was identified as a comigrator with B. terrae BS001. ► We postulate a role for biofilm formation in the migration helper effect.
Introduction
Soil is a highly structured environment in which conditions fluctuate, leading to both spatial and temporal heterogeneities in local conditions (Standing and Killham, 2007). The living soil is the “house” of a multitude of micro- and macro-organisms that show a wide array of interactions (Marschner et al., 2001, Waterfield et al., 2004). Darwinian theory dictates that each organism established in soil has its own specific niche which is defined by nutritional and spatial aspects of the microhabitat (Van Elsas et al., 2007). Our understanding of the living soil further indicates that novel soil microhabitats may be constantly formed via the movement, growth and death of organisms such as soil fungi (De Boer et al., 2005, Frey-Klett et al., 2007), filamentous or other bacteria, other organisms and plant roots (Marschner et al., 2001). This dynamism of local conditions, next to that caused by higher organisms such as earthworms (Lee, 1985) and insect larvae, strongly affects the soil microbiota. Bacteria that colonize the newly-formed microhabitats may be essential for soil functioning. For instance, they may play major roles in the degradation of organic material (Torsvik et al., 2002) as well as the breakdown of pollutants in soil (Harms and Wick, 2006). Furthermore, bacteria involved in plant growth promotion may show responses to emerging mycorrhizal fungi and thus colonize novel sites in soil (Frey-Klett et al., 2007, Garbaye, 1994, Johansson et al., 2004). Bacteria can interact with fungi in soil using different mechanisms (Nazir et al., 2010a). For instance, Pseudomonas fluorescens may use its polar flagella to anchor to mycelial surfaces (Sen et al., 1996). Recently, Toljander et al. (2006) reported that bacteria in the mycosphere differ in their ability to colonize vital and non-vital hyphae and also that bacterial attachment is influenced by the fungal host. Warmink and van Elsas (2009) provided evidence for biofilm formation and an involvement of TTSS in the interaction.
Given the fact that bacterial movement in soil is often severely restricted, reaching new microhabitats in soil via migration with soil fungi (Warmink and van Elsas, 2009) is a key phenomenon that may determine the ecological success of particular soil bacteria. For instance, the air gaps between soil particles, which pose unsurmountable barriers to the movement of (non-filamentous) soil bacteria, may be passed (Schafer et al., 1998). The use of fungal hyphae as “highways” to move to novel microhabitats has thus been hypothesized to offer a mechanism for, e.g., pollutant-degrading bacteria to reach soil areas where pollutant concentrations are elevated and they can become active (Kohlmeier et al., 2005, Wick et al., 2007), especially in unsaturated soil (Furuno et al., 2009). In a previous study by our group, migration of particular bacteria with hyphae of the saprotrophic soil fungus Lyophyllum sp. strain Karsten growing in soil microcosms was found (Warmink and van Elsas, 2009). Ten different bacterial types were selected from a total soil bacterial community, and of these, only four (Burkholderia terrae BS001, Dyella japonica BS018 and BS021 and Ralstonia basilensis BS017) could migrate as single species with the fungus (single-strain migrators). The remainder, when present as single strains, did not migrate with fungal hyphae. It was thus hypothesized that these strains depended on a so-called migration helper effect exerted by any one of the single-strain migrators for their movement.
In the current study, we investigated the influence of a selected single-strain migrator, B. terrae strain BS001, with Lyophyllum sp. strain Karsten hyphae on the bacterial community during selection for migration. We then characterized the putative migration helper effect exerted by this strain on the non-migrating strain D. japonica BS003.
Section snippets
Experimental setup
The microcosm system was constructed from a three-compartment Petri dish (Greiner Bio-one, Frickenhausen, Germany) as described earlier (Warmink and van Elsas, 2009). In short, two compartments of the Petri dish were filled with autoclave-sterilized soil from a deciduous forest near Gieterveen, The Netherlands (G soil; Warmink and van Elsas, 2008). The other compartment was filled with oat flake agar medium (15 g oat flake (local pet shop) and 15 g agar (Duchefa, The Netherlands)). The system
The influence of exogenous B. terrae BS001 on the bacterial communities developing along Lyophyllum sp. strain Karsten hyphae
A soil microbial community was obtained as a cell suspension from fresh G soil as described previously (Warmink and van Elsas, 2009). This suspension, containing about 108 cells per ml, was used, in conjunction or not with the single-strain migrator B. terrae BS001, in a microcosm experiment with sterilized G soil. Thus, the influence of the introduction of exogenous B. terrae BS001 (106 cells total) on the development of the introduced (estimated cell number 107 per g local soil) bacterial
Discussion
The ability of soil bacteria to migrate through soil via fungal hyphae represents a mechanism that can provide a great thrust to their ecological competence (Nazir et al., 2010a), as it allows them to reach new microhabitats which confer novel ecological opportunities. Bacteria with migratory capacity also seem to be primed to utilize fungal-released compounds at or behind the hyphal growth tips (Warmink and van Elsas, 2009). Our previous work identified three bacterial strains, i.e. B. terrae
Acknowledgements
We thank the University of Groningen, CEES office, for financial support for this work. Two anonymous reviewers are acknowledged for their very helpful comments.
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