Diversity,Metabolic Capabilities And Ecological Functions Of Bathyarchaeota In Marine Sediments

It has been estimated that approximately 2.9×10²99 cells reside in marine sediments,which is roughly equal to the estimate of cell abundance in seawater.But the majority of their physiology and metabolic functions remain unclear largely due to the lack of cultivated representative species in the laboratory.Archaea,as the important components in the sedimentary ecosystems,constitute a large fraction of the biomass and their abundance was found similar to that of Bacteria in marine sediments.The members of Bathyarchaeota are typical sedimentary microorganisms and widely distributed in global marine sediments,it's estimated that the cell number of Bathyarchaeota was 2 to 3.9×10²⁸,which is one of the most dominant microorganisms on earth.However,we still know little about their distribution,diversity,metabolic capabilities and ecological functions.In this work,a new pair of specific primers that target the major marine subgroups of bathyarchaeotal 16S rRNA genes was designed and showed high coverage and amplification efficiency.It can be used for testing the abundance of Bathyarchaeota in natural environments and monitoring their growth in enrichment cultures.The abundance of Bathyarchaeota among two sediment cores from the deep-sea sediments of South China Sea(SCS,from the Dongsha and Shenhu area,respectively)was determined.A strong correlation was found between the bathyarchaeotal abundance and the content of total organic carbon(TOC),suggesting an important role of Bathyarchaeota in organic matter remineralization in the sediments of SCS.Furthermore,diversity analysis revealed that subgroups Bathy-2,Bathy-8 and Bathy-10 were dominant bathyarchaeotal members of the deep-sea sediments in the SCS.Bathy-8 was found predominantly within the reducing and deeper sediment layers,while Bathy-10 occurred preferentially in the oxidizing and shallower sediment layers,implying that different bathyarchaeotal group have different niches within the sedimentary environment.In this study,we also try to enrich the members of Bathyarchaeota by adding different organic substrates(oleic acid,phenol,casein,lignin and cellulose).The bathyarchaeotal abundance increased 17 times after an incubation of 11 months by adding lignin,leaving Bathy 8 as the dominant subgroup.Lignin is an important component of terrestrial organic matter,and it belongs to the inert organic carbon which is difficult to be degraded by microbes.Our study implied that the members of Bathyarchaeota play an important role in degradating these abundant terrestrial organic matter in coastal sediments.Two genomic bins belong to Bathy-8 were constructed:Bin-L-1and Bin-L-2.The WL pathway was found in both bins,further conforming the existence of autotrophic metabolism in Bathyarchaeota.Two enzymes[4-oxalocrotonate tautomeras(praC/xylH)and catalase-peroxidase(katG)]involved in the pathway of lignin and aromatic compounds degradation were found in Bin-L-2.The process and mechanism of Bathyarcheaota in lignin degradation is not clearly explained in this study,further studies utilizing combined transcriptome,proteome and metabolome analysis are needed in the furture.Most of the bathyarcheaotal genomes contain the reduced acetyl coenzyme A pathway(also named Wood–Ljungdahl,WL)as revealed by previous studies,however no further proof is available at present.In this study,stable isotope labeled ¹³C NaHCO₃was also added while culturing,and obvious incorporation of ¹³C into bp-0,bp-1 and bp-2 was detected in the cultures with lignin.Combined analysis with the archaeal abundance and diversity data indicated that the labeled ¹³C of bp-0,bp-1 and bp-2 were produced by the members of Bathyarchaeota.Our study showed the ability of CO₂fixation by members of Bathyarchaeota when feed with lignin,and indicated their specific survival strategy:coexist of heterotrophic and autotrophic metabolism.Our study also implied that the members of Bathyarchaeota play an important role in the degradation of refractory organic carbon,while transforming inorganic carbon to organic carbon,which help to recycle carbon reservoir in marine subsurface sediments.