Phage co-transport with hyphal-riding bacteria fuels bacterial invasion in water-unsaturated microbial ecosystems

Abstract

Non-motile microbes enter new habitats often by co-transport with motile microorganisms. Here, we report on the ability of hyphal-riding bacteria to co-transport lytic phages and utilize them as "weapons" during colonization of new water-unsaturated habitats. This is comparable to the concept of biological invasions in macroecology. In analogy to invasion frameworks in plant and animal ecology, we tailored spatially organized, water-unsaturated model microcosms using hyphae of Pythium ultimum as invasion paths and flagellated soil-bacterium Pseudomonas putida KT2440 as carrier for co-transport of Escherichia virus T4. P. putida KT2440 efficiently dispersed along P. ultimum to new habitats and dispatched T4 phages across air gaps transporting ≈ 0.6 phages bacteria-1. No T4 displacement along hyphae was observed in the absence of carrier bacteria. If E. coli occupied the new habitat, T4 co-transport fueled the fitness of invading P. putida KT2440, while the absence of phage co-transport led to poor colonization followed by extinction. Our data emphasize the importance of hyphal transport of bacteria and associated phages in regulating fitness and composition of microbial populations in water-unsaturated systems. As such co-transport mirrors macroecological invasion processes, we recommend hyphosphere systems with motile bacteria and co-transported phages as models for testing hypotheses in invasion ecology.

Impact of fungal hyphae on growth and dispersal of obligate anaerobic bacteria in aerated habitats

“…Unlike in tightly packed industrial biofilms, soil fungi often develop extensively fractal mycelia that allow them to access heterogeneously distributed nutrients and carbon sources (22) and to bridge mycelial source-and sink-regions (23). Forming hyphae with lengths of ≈10 2 m g -1 in arable and up to 10 4 m g -1 in forest topsoil (19), mycelia thereby also serve as important pathways for bacterial dispersal ('fungal highways') (24) enabling the colonization of new habitats (25)(26)(27)(28), horizontal gene transfer (29), or predation (30). Expressing hydrophobic cell-wall proteins (hydrophobins), hyphae thereby overcome air-water interfaces and bridge air-filled pores with nutrient-rich aqueous zones containing little or no oxygen.…”