Unique deep-sea bacterial assemblages thriving on different natural organic matters delivered via in situ incubators

Abstract

The transport of organic matters to the deep sea constantly occurs in global oceans and in accompany with simultaneous microbial remineralization. However, little is known about the impact of fast sinking organic complex on oceanic deep ecosystem and its interactions with microbes throughout the process of sinking and settling on the sea bottom. In this report, to observe the response of indigenous microorganisms to the newly input of organic matters, we developed a series of deep-sea in situ incubators loaded on the seabed and seamount with various organic substrates of plant and animal origins. Through high-throughput sequencing, we found the bacterial communities, in situ enriched for 4–12 months, were significant different from the control groups. The bacteria of Marinifilaceae were revealed as the key members; in addition, other key decomposers including Spirochaetaceae, Psychromonadaceae, Vibrionaceae, and Moritellaceae were recruited in most assemblages, with varied abundance accordingly and diversified at the operational taxonomic unit (OTU) level. Additionally, sulphate-reducing bacteria (Desulfobulbaceae and Desulfobacteraceae) and sulphur-oxidizing bacteria (Arcobacteraceae and Sulfurovaceae) were the dominant taxa. Interestingly, PICRUSt analysis demonstrated that nitrogen fixation inside the assemblages was enriched in the enrichments with plant detritus or fatty acids. Within the assemblages stimulated by substrates short of nitrogen sources, the microbial network was dominated by cooperative relationships, whereas competition relationships overwhelmed the communities thriving on protein-rich animal tissue. These unique bacterial assemblages driven by newly input organic matters, constitute the microbial carbon pump involved in carbon, sulphur, and nitrogen cycles in oceanic interior.

Frequent Occurrence and Metabolic Versatility of Marinifilaceae Bacteria as Key Players in Organic Matter Mineralization in Global Deep Seas

“…In situ incubation was conducted with a deep-sea in situ microbial incubator (DIMI) amended with wood chips, wheat bran, fish scales, fish tissue, and fish oil (including docosahexaenoic acid [DHA] and eicosapentaenoic acid [EPA]) on a flat-topped seamount in the west Pacific Ocean (1,622 m water depth and 2.44°C), on the seafloor in the South China Sea (3,758 m water depth and 2.39°C), and on the deep-sea basin beside the southwest Indian Ridge in the Indian Ocean (4,434 m water depth and 2.35°C) for 348, 375, and 117 days, respectively ( 32 ). After that, the DIMI was autorecovered to the research vessel and the in situ enrichments were subjected to community composition analysis.…”

“…After that, the DIMI was autorecovered to the research vessel and the in situ enrichments were subjected to community composition analysis. As a result, MF bacteria were found to be prevalent and dominant in the enriched assemblages ( 32 ). Subsequently, the diversity and global distribution pattern of MF were analyzed based on our in situ data and public NCBI and IMNGS (Integrated Microbial Next Generation Sequencing) databases (see Tables S1 and S2 at https://doi.org/10.5281/zenodo.7050448 ).…”

“…S8A and B and Table S14 at https://doi.org/10.5281/zenodo.7050448 ), all of which are typically involved in strictly anaerobic fermentation for hydrogen production ( 62 ). These fermentation products can serve as carbon sources for SRB, e.g., Desulfobulbaceae and Desulfobacteraceae , which are and/ or energy sources also dominant in animal tissue and plant detritus enrichments ( 32 ).…”

“…Previously, we obtained a large number of plant detritus and animal incubation samples from the deep-sea region of the marginal sea (the South China Sea) and ocean (the Pacific Ocean and the Indian Ocean) using deep-sea in situ microbial incubators ( 32 ). In this study, we selected five representative incubation samples to further analyze the metabolic potential of MF subgroup in the in situ environment by analyzing their metagenomic and metatranscriptomic data.…”

“…We hypothesized that the microorganisms thriving on remains sunk into the deep sea may be different from the bacteria observed in the deep water column sampled with CTD cassettes, filter fractionation techniques, and sediment traps, because large pieces rich in OM do not constantly sink through the water column and settle to the seabed at every location. To identify the bacterial assemblage involved in the in situ transformation and degradation of the fast-sinking POM in the deep sea, we performed deep-sea in situ incubation amended with various natural animal and plant tissues in the seabed of the Indian Ocean (at a depth of 4,434 m), Pacific Ocean (1,622 m), and South China Sea (3,758 m) ( 32 ). Four to 12 months of deep-sea in situ incubations resulted in anaerobic environments, containing large numbers of anaerobes and facultative anaerobes, such as sulfur-oxidizing bacteria (SOB) of Arcobacteraceae and Sulfurovaceae , and sulfate-reducing bacteria (SRB) of Desulfobulbaceae and Desulfobacteraceae .…”