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.