Soil microbial community response to corrinoids is shaped by a natural reservoir of vitamin B12

Abstract

Soil microbial communities perform critical ecosystem services through the collective metabolic activities of numerous individual organisms. Most microbes use corrinoids, a structurally diverse family of cofactors related to vitamin B12. Corrinoid structure influences the growth of individual microbes, yet how these growth responses scale to the community level remains unknown. Analysis of metagenome-assembled genomes suggests corrinoids are supplied to the community by members of the archaeal and bacterial phyla Thermoproteota, Actinobacteria, and Proteobacteria. Corrinoids were found largely adhered to the soil matrix in a grassland soil, at levels exceeding those required by cultured bacteria. Enrichment cultures and soil microcosms seeded with different corrinoids showed distinct shifts in bacterial community composition, supporting the hypothesis that corrinoid structure can shape communities. Environmental context influenced both community and taxon-specific responses to specific corrinoids. These results implicate corrinoids as key determinants of soil microbiome structure and suggest that environmental micronutrient reservoirs promote community stability.

Phylogenetic distribution and experimental characterization of corrinoid production and dependence in soil bacterial isolates

“…5B , Supplementary Table 6 ), suggesting that these isolates have the capacity to provide sufficient or excess corrinoid to all of the dependents in our collection. Thus, our measurements of corrinoid production and providing, in the artificial conditions of laboratory culture, coupled with prior genomic studies [ 25 , 26 ], support our hypothesis that corrinoid sharing can occur within the communities of this soil.…”

“…The concentration of corrinoid chosen for the isolation media was 4-fold higher than the highest EC 50 and over 16 000-fold higher than the lowest EC 50 we measured, which explains why isolates were often recovered in their non-preferred corrinoid and why we detected no taxonomic trends in the corrinoid used for isolation. Despite the presence of excess corrinoid in our isolation media, we recovered fewer corrinoid-dependent isolates than expected [ 26 , 50 ], which may be due to corrinoid-dependent bacteria having additional nutrient dependencies not satisfied by our isolation medium or requiring specific partners for their survival. Indeed, in an analysis of auxotrophies in gut microbiome genomes, most predicted B12 auxotrophs had at least one other vitamin auxotrophy, [ 6 ] and among a set of marine isolates, 10/13 B12 auxotrophs were also auxotrophic for at least one other B vitamin [ 67 ].…”

“…3 ). The abundance of producers E in our collection contrasts with genome-based predictions that dependents outnumber producers across bacteria and specifically in soil [ 25 , 26 , 50 ].…”

“…1B ) [ 25 ]. Given that dependents and producers coexist in the same environments [ 26–28 ], we hypothesize that many sharing interactions have yet to be described.…”