Biogeographic distributions of microbial communities associated with anaerobic methane oxidation in the surface sediments of deep-sea cold seeps in the South China Sea

Abstract

Cold seeps are oasis for the microbes in the deep-sea ecosystems, and various cold seeps are located along the northern slope of the South China Sea (SCS). However, by far most microbial ecological studies were limited to specific cold seep in the SCS, and lack of comparison between different regions. Here, the surface sediments (0–4 cm) from the Site F/Haima cold seeps and the Xisha trough in the SCS were used to elucidate the biogeography of microbial communities, with particular interest in the typical functional groups involved in the anaerobic oxidation of methane (AOM) process. Distinct microbial clusters corresponding to the three sampling regions were formed, and significantly higher gene abundance of functional groups were present in the cold seeps than the trough. This biogeographical distribution could be explained by the geochemical characteristics of sediments, such as total nitrogen (TN), total phosphorus (TP), nitrate (NO3−), total sulfur (TS) and carbon to nitrogen ratios (C/N). Phylogenetic analysis demonstrated that mcrA and pmoA genotypes were closely affiliated with those from wetland and mangroves, where denitrifying anaerobic methane oxidation (DAMO) process frequently occurred; and highly diversified dsrB genotypes were revealed as well. In addition, significantly higher relative abundance of NC10 group was found in the Xisha trough, suggesting that nitrite-dependent DAMO (N-DAMO) process was more important in the hydrate-bearing trough, although its potential ecological contribution to AOM deserves further investigation. Our study also further demonstrated the necessity of combining functional genes and 16S rRNA gene to obtain a comprehensive picture of the population shifts of natural microbial communities among different oceanic regions.

Active pathways of anaerobic methane oxidization in deep-sea cold seeps of the South China Sea

“…A similar phenomenon has also been observed in the pockmark ( 8 ) and Thuwal cold seeps ( 53 ), with the potential influence of sulfate concentrations ( 54 ). Highly diversified substrates utilizing capabilities of different SRB groups found in our study reflected a better adaptability to the deep-sea environment ( 55 ), and a potentially higher ecological contribution to AOM progress in the cold seeps and trough ( 20 ). Though SAMO was the main CH 4 removal pathway in marine habitats ( 21 ), a greater contribution of DAMO to CH 4 sink was reported in the Zhoushan intertidal zone ( 25 ).…”

“…This cluster was closely related to sequences recovered from Yangtze Estuary sediments ( 26 ) and Indonesian river sediments ( 39 ), which are typical habitats for the occurrence of Nr-DAMO processes ( 13 ). As for the pmo A gene, two distinct clusters formed, with Cluster I closely related to sequences recovered from the sediments of the SCS ( 18 , 64 ), in which NC10 bacteria have been identified ( 18 , 19 ) and their associated N-DAMO process has been proposed as well ( 20 ). The relative abundance of Cluster I was higher in the 13 CH 4 + NO 2 − treatment groups of the cold seeps than the trough.…”

“…More recently, the bacterium Candidatus Methylomirabilis oxyfera ( M. oxyfera, NC10) can couple AOM to nitrite reduction through an intra-aerobic methane oxidation pathway (known as “nitrite-dependent AOM” or N-DAMO) ( 12 ), and a novel ANME lineage named Candidatus Methanoperedens nitroreducens (ANME-2d) population can perform nitrate-driven AOM pathway (known as “nitrate-dependent AOM” or Nr-DAMO) ( 13 , 14 ) was revealed. These DAMO-related microbial groups have been identified in the sediments collected from mangroves ( 15 , 16 ), freshwater sources ( 13 , 17 ), the continental shelf, and cold seeps of the South China Sea (SCS) ( 18 – 20 ), suggesting the DAMO process might occur widely in aquatic environments. Nevertheless, the research on Nr-/N-DAMO in aquatic habitats is still very limited so far.…”

“…The microbial communities (ANME and SRB) have been investigated ( 6 , 7 , 30 ), and rates of AOM and sulfate reduction were measured recently with 14 C or 35 S labeled tracers separately ( 31 ). In the last decade, microbial groups involved in the DAMO process were also identified based on the presence of 16S rRNA gene and functional genes ( pmo A, mcr A, and dsr B) in the cold seeps and the Xisha trough in SCS ( 18 – 20 ). However, detection of the DAMO-related microbes at the DNA level does not guarantee the occurrence of this process, and the role of these microbial groups in the AOM processes needs to be further investigated.…”

The diversification and potential function of microbiome in sediment-water interface of methane seeps in South China Sea

“…The association of ANME-2d archaea and NC10 bacteria with the DAMO process has been proposed from the coastal mangrove wetland to the South China Sea sediments ( Chen et al, 2022 ). Nitrite-dependent DAMO process is more important in the hydrate-bearing trough ( Jiang et al, 2022 ). The relative abundance of Methylomonadaceae (o_Methylococcales) is highest in the methane seep/bio-luxuriance zone among these microenvironments, where the methane concentration can exceed 31,200 ppm (∼55.2 μM), and DO ranges from 0 to 3.3 mg/L.…”