A diverse uncultivated microbial community is responsible for organic matter degradation in the Black Sea sulphidic zone

Abstract

Organic matter degradation in marine environments is essential for the recycling of nutrients, especially under conditions of anoxia where organic matter tends to accumulate. However, little is known about the diversity of the microbial communities responsible for the mineralization of organic matter in the absence of oxygen, as well as the factors controlling their activities. Here, we determined the active heterotrophic prokaryotic community in the sulphidic water column of the Black Sea, an ideal model system, where a tight coupling between carbon, nitrogen and sulphur cycles is expected. Active microorganisms degrading both dissolved organic matter (DOM) and protein extracts were determined using quantitative DNA stable isotope probing incubation experiments. These results were compared with the metabolic potential of metagenome-assembled genomes obtained from the water column. Organic matter incubations showed that groups like Cloacimonetes and Marinimicrobia are generalists degrading DOM. Based on metagenomic profiles the degradation proceeds in a potential interaction with members of the Deltaproteobacteria and Chloroflexi Dehalococcoidia. On the other hand, microbes with small genomes like the bacterial phyla Parcubacteria, Omnitrophica and of the archaeal phylum Woesearchaeota, were the most active, especially in protein-amended incubations, revealing the potential advantage of streamlined microorganisms in highly reduced conditions.

Microbiome of the Black Sea Water Column Analyzed by Genome Centric Metagenomics  

“…The present study, together with others from the same Black Sea [5,8] (bioproject PRJNA649215) and those recent ones from the Cariaco Basin in Venezuela [21,23] show a rst glimpse on the microbiome of anoxic marine water columns. The redoxclines of these habitats show a convergence of various metabolisms at a time, among which we encounter anoxygenic photosynthesis such as that one observed in Chlorobium phaeobacteroides [24], ammonia oxidation by Nitrosopumilus spp., chemolithotrophic metabolisms carried by Gammaproteobacteria such Ca.…”

“…Although a few studies have been carried out by metagenomics and metagenome-assembled genomes (MAGs) reconstruction, the information available in databases about this unique environment is scarce. A recent study showed for the rst time the microbial structure of the sul dic waters of 1000 m depth [5], mainly dominated by sulfate reducers (Desulfobacterota and Chloro exi classes such as Dehalococcoidia or Anaerolinea), associated DOM degraders (Marinimicrobia, Cloacimonetes) and streamlined uncultured taxa such as Omnitrophica, Parcubacteria or Woesearchaeota. At the genome level, Black Sea microbes remain largely unknown.…”

Microbial Processes and Microbial Communities in the Water Column of the Polar Meromictic Lake Bol’shie Khruslomeny at the White Sea Coast

“…Abundance of these organisms indicates that they may play an important ecological role. Thus, it was recently shown that Woesearchaeota and Patescibacteria form an important part of the protein-degrading microbial communities in the Black Sea anoxic waters ( Suominen et al, 2019 ). Moreover, due to a higher ratio of surface area to volume, small cell size facilitates nutrient uptake and increases the metabolic rate ( Savage et al, 2007 ).…”

“…Analysis of the genomes of these microorganisms revealed their ability to utilize proteinaceous substrates (Pelletier et al, 2008), cellulose (Limam et al, 2014), and propionate (Nobu et al, 2015), as well as to form syntrophic associations with other microorganisms (Dyksma and Gallert, 2019). Cloacimonetes were revealed in various anaerobic ecosystems, including the Black Sea sulfide zone, where they were found to be responsible for degradation of dissolved organic matter (Suominen et al, 2019). The highest share of Cloacimonetes (8-13%) occurred at the depths below 7 m. The closest relatives have been found in the sediments of meromictic lakes and in Pacific hydrothermal vents.…”

Assessing the Effect of Humic Substances and Fe(III) as Potential Electron Acceptors for Anaerobic Methane Oxidation in a Marine Anoxic System

“…Another filter was directly stored at −80 °C for analysis of the in situ microbial community. Water column samples for nutrient and DNA analysis were collected as described in Sollai et al (2019) and Suominen et al (2020) [ 30 , 33 ].…”