Interplay between microbial community composition and chemodiversity of dissolved organic matter throughout the Black Sea water column redox gradient

Abstract

Large quantities of carbon are stored in marine dissolved organic matter (DOM), and its recycling has a major effect on the carbon cycle. Microbes are responsible for turnover of DOM. Little is known about how the complex pool of DOM shapes microbial communities and vice versa, especially in anoxic systems. In this study, we characterized the DOM pool with high-resolution Fourier transform ion cyclotron resonance mass spectrometry and analyzed the microbial community composition with 16S rRNA gene amplicon sequencing across a redox gradient in the Black Sea. The chemical stratification of the water column was clearly reflected in the microbial community, with different putative autotrophic taxa abundant across redox zones. The nitrate maximum was characterized by a high abundance of Thaumarchaeota, the suboxic zone by Gammaproteobacteria Chromatiales, while Epsilonbacteraeota Campylobacterales were abundant at the onset of the sulfidic zone. Compared to the variance in the microbial community, the molecular composition of DOM was relatively uniform across the sampled depths. However, underlying differences in the oxidation state of the DOM molecular formulas showed distinct changes that were linked to the redox zones, possibly connecting autotrophic metabolisms to changes in the DOM composition. In addition, known heterotrophs like Planctomycetes Phycisphaerae and Chloroflexi Anaerolineales were linked to more oxidized molecular forms of DOM, and not to the identified redox zones, suggesting that these fermentative organisms are reliant on newly formed carbon molecules. Our study suggests that the metabolism of autotrophic microbes influences the composition of DOM across the Black Sea water column.

Organic matter degradation in the deep, sulfidic waters of the Black Sea: Insights into the ecophysiology of novel anaerobic bacteria

“…Based on these results and earlier work 4,5,8,9,13–15 , it is anticipated that Psychrilyobacter spp., members of the order Clostridiales (closely related to strains A1 T and A2), Marinifilaceae members (closely related to A. euxinus and L. euxinus ), Lutibacter spp. (closely related to strains B1 T and B2) and Lentimicrobiales members (related to strains S6 and L6), Sphaerochaeta spp.…”

“…Based on these results and earlier work 4,5,8,9,[13][14][15] , it is anticipated that Psychrilyobacter spp., members of the order Clostridiales (closely related to strains A1 T Izemo-BS could be key anaerobes involved in the turnover of "fresh" and labile OM (i.e., carbohydrates, proteins, lipids and nucleic acids) passaging through the deep sulfidic waters of the Black Sea.…”

“…Members of the phylum Mycoplasmatota are also present in deep marine habitats and have been identified as specialized degraders of DNA 5,[8][9][10] . In addition to these key taxa, there are also other microbial members affiliated with the phyla Bacteroidota (especially Marinifilaceae, Marinilabiaceae, Lentimicrobiaceae), Desulfobacterota (especially Desulfovibrionaceae, Desulfobacteraceae, Desulfobulbaceae), Planctomycetota (Phycisphaerae), Ignavibacteriota, Chloroflexota (Anaerolineae), Cloacimonadota, and Nanoarchaeota, which have been predicted to be involved in OM degradation in deep marine habitats 4,5,7,[11][12][13][14][15] . Although the identity and potential functions of these microbial taxa are known, their physiology remains largely unknown due to the limited availability of isolated representatives and enrichment cultures.…”

“…Additionally, the concentration of dissolved organic carbon (DOC) in the Black Sea is about 2.5 times higher than in any of the major ocean basins [17][18][19] . Recent studies by Suominen et al [13][14][15] focused on the role of uncultivated microbial communities in OM degradation in the deep sulfidic waters of the Black Sea, concluding that members of the Gammaproteobacteria, Alphaproteobacteria, Bacteroidota, and Planctomycetota thrive in incubations with complex carbon sources, such as chitin and peptidoglycan, while members of the phyla Planctomycetota, Latescibacteria, Kirimatillaeota, Cloacimonadota, Nanoarchaeota, and Chloroflexota also do so in incubations with fatty acids 13,14 . However, detailed investigations of the physiology of these microbial groups and their adaptation strategy are still lacking.…”

Organic matter degradation in the deep, sulfidic waters of the Black Sea: Insights into the ecophysiology of novel anaerobic bacteria

“…Members of the phylum Mycoplasmatota are also present in deep marine habitats and have been identi ed as specialized degraders of DNA [5,[8][9][10]. In addition to these key taxa, there are also other microbial members a liated with the phyla Bacteroidota (especially Marini laceae, Marinilabiaceae, Lentimicrobiaceae), Desulfobacterota (especially Desulfovibrionaceae, Desulfobacteraceae, Desulfobulbaceae), Planctomycetota (Phycisphaerae), Ignavibacteriota, Chloro exota (Anaerolineae), Cloacimonadota, and Nanoarchaeota, which have been predicted to be involved in OM degradation in deep marine habitats [4,5,7,[11][12][13][14][15]. Although the identity and potential functions of these microbial taxa are known, their physiology remains largely unknown due to the limited availability of isolated representatives and enrichment cultures.…”