Composition,Metabolic Characteristics And Important Biogeochemical Processes Of Microbes In The Water Column Of The Oligotrophic South China Sea

Marine organic matter is one of the largest carbon reservoir on earth,which is crucial for the oceanic and global carbon cycle.The ocean’s water column is full of ’hot spots’ organic particles,which serve as the microhabitats for microorganisms.The particles can attract chemotactic bacteria to attach to the surface.The composition and life strategies of the particle-attached(PA)microbes are very different from that of freeliving(FL)microbes.For the two lifestyle microbial communities,the structure,metabolic characteristics and the biogeochemical processes that they are involved in have become the focus of marine research.In the oligotrophic open ocean,there are three regimes through the water column according to the light transmission intensity:the euphotic zone(0-200 m),the twilight zone(200 m to 1,000 m)and the bathypelagic zone(deeper than 1,000 m).The euphotic zone is the dominant realm of organic matter production.A significant proportion of the organic matter produced in the sunlit region is exported into the deep sea as sinking particles.The sinking particles not only fuel the generally starved bathypelagic microbes,but also have impacts on the ecology and assembly of deep ocean microbial communities.The deep sea is the dark end of the carbon pump,where the sinking particles are buried to the seabed after the final transformation and remineralization.The deep-sea microbial respiration contributes one-third of the total CO2 production in the ocean,indicating that the metabolism of microbes is active in this realm,however,we know little about it.This dissertation focused on the microbes in the water column of the oligotrophic South China Sea.We collected samples from five layers in the vertical direction:5 m,deep chlorophyll maximum(DCM)layer,200 m,750 m and 3,000 m.A sizefractionated sampling strategy was adopted to collected both 0.2-1.6 μm and 1.6-200μm microbial samples.By integrating the metaproteomic,metagenomic,16S rRNA sequencing and bioinformatics analysis,we studied key microbial players and important biological processes in the water column.Furthermore,we revealed the microbial functional vertical connectivity throughout the water column and the mechanisms involved in the organic matter remineralization.The main results were as follows:(1)In the oligotrophic euphotic SCS,the composition and metabolic characteristics of microbial functional groups were significantly different between the upper nutrientdepleted layer(NDL)and the lower nutrient-replete layer(NRL).Rhodobacterales,Alteromonadales and Oceanospirillales were the dominant prokaryotic functional groups,however,their relative abundance significantly differed between the two regimes.The protein abundance of eukaryotic phytoplankton increased from NDL to NRL,indicating a more important metabolic role in the NRL.Two cyanobacterial genus Synechococcus and Prochlorococcus adopted a mixotroph strategy,and they transported and utilized urea and amino acids as their organic nitrogen sources.Freeliving proteobacterial members along with the mixotrophic picocyanobacteria were the predominant carbon fixers in the NDL.However,microbial CO2 assimilation was more active in the NRL and the eukaryotic phytoplankton significantly contributed to the carbon fixation in this regime.(2)Microbial composition and function exhibited a strong vertical connectivity between the surface and the deep ocean.The large sinking particles were the important vector that transported viable surface microbes to the deep ocean,which mostly influenced the function of the bathypelagic PA communities but also the deep-sea FL assemblages.Oceanospirillales,Alteromonadales and Rhodobacterales were the key groups that mediated the functional vertical connectivity between surface and bathypelagic microbial communities.They were also the dominant groups that drove the remineralization of organic matter in the water column.During the immigration from surface to the deep sea,those surface microbes developed their unique environmental adaptation mechanisms through maintaining the high stability of basal metabolism such as cell growth,transcription and translation,improving the transport and utilization efficiency of organic matter as well as initiating different defensive responses to various environmental stresses such as temperature,starvation,hypertonicity and reactive oxygen species.Thus,they could survive in the changing water column environments and colonize in the bathypelagic zone.(3)The organic matter processing strategies of PA and FL microbes were different in the bathypelagic SCS.The PA prokaryotes expressed diverse extracellular hydrolytic enzymes and played the central role in organic matter remineralization,while the FL microbes predominantly lived on the solubilized substrates cleaved from particles.Alteromonadales,Oceanospirillales and Sphingomonadales could utilize the lowbioavailability organic compounds as carbon source by expressing high abundant monooxygenase,dioxygenase,dehydrogenase as well as a few classes of hydrolase.Such bacterial groups performed a ’sharing’ mode of organic matter processing,contributing large amounts of hydrolytic enzymes to facilitate the particle organic matter solubilization.Meanwhile,other ’self-focusing’ bacterial groups,such as Pelagibacterales and Rhodobacterales within Alphaproteobacteria produced none or less specific enzymes but expressed high abundance of transporters to assimilate diverse available substrates in the bathypelagic zone.In general,this study applied a combination of metaproteomic,metagenomic,16S rRNA sequencing and bioinformatics analysis to study the microbial composition and metabolic characteristics in the oligotrophic water column,revealing the microbial compositional and functional vertical connectivity as well as the organic matter remineralization mechanism in the oligotrophic ocean,and obtaining a new understanding of microbial remineralization of organic matter.This study not only enriches the research contents of marine organic matter biogeochemistry and deep-sea microbial ecology,but also provides an example for subsequent related research.