Phage co-transport with hyphal-riding bacteria fuels bacterial invasion in a water-unsaturated microbial model system

Xin You,Hauke Harms,Lukas Y Wick,Matthias Schmidt,Ingolf Kühn,Antonis Chatzinotas,René Kallies

doi:10.1038/s41396-021-01155-x

Abstract

Nonmotile microorganisms often enter new habitats by co-transport with motile microorganisms. Here, we report that also lytic phages can co-transport with hyphal-riding bacteria and facilitate bacterial colonization of a new habitat. 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 seems analogous to macroecological invasion processes, hyphosphere systems with motile bacteria and co-transported phages could be useful models for testing hypotheses in invasion ecology.

Highlights

To cope with the heterogeneous and highly changeable soil environment, microorganisms have evolved inter-microbial cotransport strategies to gain motility and colonize new habitats
Being a prerequisite for phage co-transport with carrier bacteria we tested the adsorption of T4 phages to the flagellated WT of P. putida KT2440 and its non-flagellated ΔfilM mutant
For co-transported phages, time-dependent transport capacity (Cp, Plaque forming unit (PFU) bacteria−1) reflect the average number of phages transported by a single bacterium and transport efficiency (Ep, %) the fraction of phages dispatched by carrier bacteria

Summary

Introduction

To cope with the heterogeneous and highly changeable soil environment, microorganisms have evolved inter-microbial cotransport strategies to gain motility and colonize new habitats (reviewed by [1]). Fungi embody up to 75% of the subsurface microbial biomass [5] Their hyphae create fractal-like mycelial networks of 102–104 m g−1 of topsoil and efficiently spread in heterogeneous habitats, penetrate air-water interfaces and cross over air-filled pores [5,6,7]. They thereby serve as pathways ( called “fungal highways” [2]) for bacteria to efficiently disperse, forage [8] and colonize new habitats [4, 9]. In unsaturated environments like soil, little is known about cotransport of phage with motile bacteria and the associated effect on bacterial population dynamics

Methods

Results

Conclusion