The frequent occurrence and metabolic versatility of Marinifilaceae bacteria involved in organic matter mineralizationas a key member in global deep sea

Abstract

Transfer of animal and plant detritus of both terrestrial and marine origins to the deep sea occurs on the global scale. Microorganisms play an important role in mineralizing them therein, yet to identify in situ. Here we report the family Marinifilaceae that occurred as one of the most predominant bacteria thriving on the new inputs of plant and animal biomasses in both marginal and oceanic areas observed via in situ incubation about their differentiation, environmental adaption, and metabolic mechanisms underlying their prevalence in organic matter mineralizing communities. We described the metabolic features and in situ metabolizing activities of different subgroups (tentative genus level), based on the metagenomic and metatranscriptomic data. One representative subgroup MF-2 dominated plant detritus-enriched cultures and specialized in polysaccharide degradation by encoding many hydrolases involved in the hydrolysis of hemicellulose, pectin, starch, cellulose, and polysaccharides containing N-acetyl groups; this subgroup also encodes a manganese superoxide dismutase with the potential of lignin oxidation and possesses complete nitrogen fixation pathway to compensate for the shortage of nitrogen sources inside the plant detritus. In contrast, those dominating the animal tissue-supported microbiomes were more diverse and formed three subgroups, which distinguished themselves from MF-2 in carbon and nitrogen metabolisms. Regardless of differentiation in carbon and nitrogen metabolisms, they share in common in energy conservation through organic fermentation, and anaerobic respiration of diverse electron receptors. These results highlight the role of Marinifilaceae bacteria neglected before in organic matter mineralizing in marine environments coupling carbon and nitrogen cycling with metals and other elements. IMPORTANCEMicrobial mineralization of organic matters has a significant impact on the global biogeochemical cycle. This report confirmed the role of Marinifilaceae in organic degradation in the oceans, with underestimated contribution in the ocean carbon cycling. It is the dominant taxon thriving on plant and animal biomasses in our in situ incubator, as well as in whale- and wood-falls. At least nine subgroups were revealed, and widely distributed in global oceans but merely predominant in organic-rich environments with an average relative abundance of 8.3 %. Different subgroups display a preference for the degradation of different macromolecules (polysaccharides, lignin, and protein) and adapt themselves to the environments via special metabolic metabolisms.