Structures And Metabolic Profiles Of The Microbial Communities Inhabiting The Sediments In Okinawa Trough And Manus Basin

Deep-sea hydrothermal environment is one of natural extreme environments on Earth.However,it harbors active ecosystems.Submarine hydrothermal environments have been considered as a possible site for the origin and early evolution of life on Earth.Hydrothermal systems attract the attentions of scientists from different research fields.Okinawa Trough and Manus Basin,both located in the western Pacific Ocean,are two typical back-arc basins,which are active in different expansion phases.Although previous studies have provided insights into the geological settings and geochemistry of hydrothermal fluids in the two regions,little is known about the microbial ecosystems inhabiting the sediments from the hydrothermal fields.Hydrothermal field investigations were conducted by the scientific research vessel “KEXUE” in Iheya North and Iheya Ridge of mid-Okinawa Trough and in Pacmanus and Desmos of eastern Manus Basin.Deep-sea sediment samples were collected during the two cruises,which provide us precious materials for the research of submarine hydrothermal microbial ecosystems.Eight sediment samples were used in the current study,and taxonomic compositions,metabolic profiles and potential energy sources of microbial communities were analyzed,aiming to illustrate microbial adaptation strategies to deep-sea hydrothermal environments.The results showed that there were high microbial diversities in the microbial communities inhabiting the sediments of Iheya North,Iheya Ridge,Pacmanus and Desmos hydrothermal fields.All the microbial communities were dominated by bacteria and,to a lesser extent,archaea.Proteobacteria,especially Alpha-and Gammaproteobacteria,were the dominant bacterial populations in these microbial communities.Euryarchaeota was the dominant archaeal population in the microbial communities from Iheya North and Iheya Ridge,which was an important participant in methane metabolism;Thaumarchaeota,involved in ammonia oxidization,was the predominant archaeal population in the microbial communities from Pacmanus and Desmos.Chemolithoautotrophic microorganisms were primary producers in all the microbial communities.The important members of the autotrophs included ammonia-oxidizing bacteria and archaea,nitrite oxidizer,sulfur oxidizer and methanogens,which can assimilate CO₂ via various carbon fixation pathways thereby producing organic matters.Ammonia,nitrite,hydrogen and reduced sulfur compounds as important energy sources fueled the microbial communities in the sediment habitats of mid-Okinawa Trough and eastern Manus Basin.Methane was a potential energy source for microorganisms inhabiting Iheya hydrothermal fields;anaerobic methane-oxidizing archaea and bacteria,likely oxidizing methane through reverse methanogenesis coupled to nitrate reduction and “intra-aerobic denitrification” respectively,were found in the communities.In the eight microbial communities,nitrification and denitrification were primary nitrogen metabolic processes,and sulfate reduction and sulfur-oxidizing reverse sulfate reduction were primary sulfur metabolic processes.Nitrate and sulfate as important electron acceptors were utilized by microorganisms.In this study,taking samples of Iheya North and Iheya Ridge hydrothermal fields as an example,we tried to illustrate how the microbial communities constructed and operated in deep-sea sediments.An assumption was made on the basis of metabolic profiles of the microbial communities as revealed by metagenomics in this study and a reference model of early diagenetic process in marine sediments.We think that small molecules which originated from the decomposition of organic matters promoted the formation of microbial communities and that methane metabolism as a power drove the carbon,nitrogen and sulfur cycling and the ecosystem operation.The microorganisms in the microbial communities were predicted to distribute in different sediment layers to deal with the needs for oxygen and nutrients,substrate inhibition,and microbial consortium.This study contributed to shed light on microbial adaptation strategies to deepsea sedimental environments.DNA repair system represented a survival mechanism for submarine microorganisms,which could cope with the damaging effects on the genomes caused by the harsh environments,thereby maintaining microbial primary structures of nucleic acids.In addition,there were other microbial adaptation strategies to regulate osmoadaptation and pH homeostasis,such as changing the contents of cardiolipin and phosphatidylglycerol in membrane lipids,controlling the concentrations of polyamines,Na⁺,K⁺ and osmoprotectants?e.g.,glycine betaine,proline,trehalose?via various ABC-transporting systems,cation:proton antiporters and mechanosensitive channels.Many findings in this study are for the first time among the relevant researches about microbial ecosystems in the sediment habitats surrounding Iheya North,Iheya Ridge,Pacmanus and Desmos hydrothermal fields.The results of this study facilitate our understanding the formation and operation of submarine microbial communities,unveil the adaptation mechanisms of deep-sea microorganisms,and add insights into the recognition of deep-sea hydrothermal ecosystems.