Transient exposure to oxygen or nitrate reveals ecophysiology of fermentative and sulfate-reducing benthic microbial populations

Abstract

Conflict of interestThe authors declare no conflict of interest.\n\nShort summaryFermentation coupled to sulfate reduction is a globally important process for the remineralization of organic carbon in marine sediments. The present study uses long-term, replicated continuous culture bioreactors and meta-omics to investigate the ecophysiology of the involved microbial populations at an unprecedented resolution. We reveal complex trophic networks, in which fermenters and sulfate reducers coexist with nitrate- and oxygen respirers, we indicate strategies and niches of the microbial populations, and describe a novel and widespread, yet uncultured fermentative organism. These insights are crucial to understand fermentation coupled to sulfate reduction and relevant to assess microbial dynamics and community-level responses in coastal ecosystems.\n\nFor the anaerobic remineralization of organic matter in marine sediments, sulfate reduction coupled to fermentation plays a key role. Here, we enriched sulfate-reducing/fermentative communities from intertidal sediments under defined conditions in continuous culture. We transiently exposed the cultures to oxygen or nitrate twice daily and investigated the community response. Chemical measurements, provisional genomes and transcriptomic profiles revealed trophic networks of microbial populations. Sulfate reducers coexisted with facultative nitrate reducers or aerobes enabling the community to adjust to nitrate or oxygen pulses. Exposure to oxygen and nitrate impacted the community structure, but did not suppress fermentation or sulfate reduction as community functions, highlighting their stability under dynamic conditions. The most abundant sulfate reducer in all cultures, related to Desulfotignum balticum, appeared to have coupled acetate oxidation to sulfate reduction. We described a novel representative of the widespread uncultured phylum Candidatus Fermentibacteria (formerly candidate division Hyd24-12). For this strictly anaerobic, obligate fermentative bacterium, we propose the name Ca. \"Sabulitectum silens\" and identify it as a partner of sulfate reducers in marine sediments. Overall, we provide insights into the metabolic network of fermentative and sulfate-reducing microbial populations, their niches, and adaptations to a dynamic environment.