Novel microbial syntrophies identified by longitudinal metagenomics

Identifying species interactions in a microbial community and how this relates to community function is a key challenge. Towards addressing this challenge, we present here an extensive genome-resolved, longitudinal dataset and associated metadata. We collected weekly samples of microbial communities and recorded operating conditions from industrial methane producing anaerobic digestion reactors for a year. This allowed us to recover 2240 dereplicated metagenome assembled genomes (dMAGs), together with their coverage dynamics and functional annotations from which functional traits were inferred. Of these dMAGs, 1910 were novel species, with 22 representing novel orders and classes. Methanogenic communities are expected to be strongly structured by syntrophic and other associations between the methanogens and syntrophs that produce their substrates. We identified 450 potential syntrophic dMAGs by searching for pairs of methanogenic and non-methanogenic dMAGs that had highly correlated time-series. Genomes of potential syntrophs were enriched for oxidoreductases and sugar transport genes and there was a strong taxonomic signal in their associations with methanogens. Of particular note, we found that Bathyarchaeiea associated specifically with methanogens from the Thermoplasmata, and Thermococci classes. Same syntrophic associations were only rarely observed across multiple reactors, suggesting that syntrophies might be facultative, with particular strains within a species forming syntrophic associations only sometimes and not necessarily always with the same methanogenic partner. The presented results show that longitudinal metagenomics is a highly valuable approach for identifying species and their interactions in microbial communities.

Syntrophic Growth on Formate: a New Microbial Niche in Anoxic Environments

ABSTRACT Anaerobic syntrophic associations of fermentative bacteria and methanogenic archaea operate at the thermodynamic limits of life. The interspecies transfer of electrons from formate or hydrogen as a substrate for the methanogens is key. Contrary requirements of syntrophs and methanogens for growth-sustaining product and substrate concentrations keep the formate and hydrogen concentrations low and within a narrow range. Since formate is a direct substrate for methanogens, a niche for microorganisms that grow by the conversion of formate to hydrogen plus bicarbonate—or vice versa—may seem unlikely. Here we report experimental evidence for growth on formate by syntrophic communities of (i) Moorella sp. strain AMP in coculture with a thermophilic hydrogen-consuming Methanothermobacter species and of (ii) Desulfovibrio sp. strain G11 in coculture with a mesophilic hydrogen consumer, Methanobrevibacter arboriphilus AZ. In pure culture, neither Moorella sp. strain AMP, nor Desulfovibrio sp. strain G11, nor the methanogens grow on formate alone. These results imply the existence of a previously unrecognized microbial niche in anoxic environments.