Impact of spatial organization on a novel auxotrophic interaction among soil microbes

Abstract

A key prerequisite to achieve a deeper understanding of microbial communities and to engineer synthetic ones is to identify the individual metabolic interactions among key species and how these interactions are affected by different environmental factors. Deciphering the physiological basis of species–species and species–environment interactions in spatially organized environments requires reductionist approaches using ecologically and functionally relevant species. To this end, we focus here on a defined system to study the metabolic interactions in a spatial context among the plant-beneficial endophytic fungus Serendipita indica, and the soil-dwelling model bacterium Bacillus subtilis. Focusing on the growth dynamics of S. indica under defined conditions, we identified an auxotrophy in this organism for thiamine, which is a key co-factor for essential reactions in the central carbon metabolism. We found that S. indica growth is restored in thiamine-free media, when co-cultured with B. subtilis. The success of this auxotrophic interaction, however, was dependent on the spatial and temporal organization of the system; the beneficial impact of B. subtilis was only visible when its inoculation was separated from that of S. indica either in time or space. These findings describe a key auxotrophic interaction in the soil among organisms that are shown to be important for plant ecosystem functioning, and point to the potential importance of spatial and temporal organization for the success of auxotrophic interactions. These points can be particularly important for engineering of minimal functional synthetic communities as plant seed treatments and for vertical farming under defined conditions.

Genome and evolution of the arbuscular mycorrhizal fungus Diversispora epigaea (formerly Glomus versiforme) and its bacterial endosymbionts

“…irregularis (Tisserant et al ., ; Lin et al ., ; Wewer et al ., ). Loss of thiamine biosynthesis has been observed in several fungi (Jiang et al ., ), and at least one of the biosynthetic enzymes is enzymatically costly, so loss of the pathway may be advantageous in certain environments. Interestingly, Serendipita indica , a thiamine auxotroph and endophyte of plants, can use thiamine provided by either plants or bacteria (Jiang et al ., ).…”

The social network of microorganisms — how auxotrophies shape complex communities

“…Computational and in vivo studies have shown that spatial structure of microbial communities is a determining factor for cooperation and can drive community dynamics 16,52,53 . Co-culture experiments involving Bacillus subtilis and the endophytic fungus Serendipita indica revealed that thiamine (vitamin B 1 ) is a key nutrient for the B 1 auxotroph S. indica .…”

A riboswitch gives rise to multi-generational phenotypic heterogeneity in an auxotrophic bacterium

“…Indeed, multiple studies have shown how syntrophic cross-feeding interactions, based on the reciprocal exchange of amino acids, lead to stable coexistence 2,7 . Auxotrophies are therefore likely to play a prominent role in determining the composition and stability of microbial communities [8][9][10] .…”