Biogeographic Traits And Ecological Functions Of Important Organosulfur Catabolism Driven By Marine Bacteria In Polar Oceans

Dimethyl sulfide(DMS)is an important participant in the global sulfur cycle,and potentially involved in global climate regulation.Dimethylsulfoniopropionate(DMSP)is the predominant source of oceanic DMS,and also one of the most abundant organic sulfur compounds in the marine environment.Microorganisms are major players in driving the marine DMS/DMSP cycle.The production and consumption processes of microorganisms have an important effect on the fluxes of DMS and DMSP in the ocean.In addition to participating in the global sulfur cycle and climate regulation,DMS/DMSP also plays many important physiological and ecological functions.It has been reported that DMSP cleavage plays an important role to deter herbivores in DMSP-producing eukaryotic algae.However,whether a parallel DMSP cleavage system operates in marine bacteria to defend against predators remains elusive.Polar oceans represent approxinamtly one fifth of Earth's surface,and and play an important role in the global climate system.High concentrations of DMS/DMSP have been reported in both the Arctic Ocean and the Southern Ocean.With the global warming threat,the polar regions are experiencing rapid changes including sea ice melting that is known to correlate with the reduced production of DMS/DMSP,which in turn,may feedback to the global climate.Thus,interpreting the biogeographic traits of DMS/DMSP cycling in Arctic and Antarctic oceans is an urgent task.In this study,we systematically investigated the biogeographic traits of 16 key microbial enzymes involved in DMS/DMSP cycling in 60 metagenomic samples from polar waters,together with 174 metagenome and 151 metatranscriptomes from non-polar Tara Ocean dataset.Our study provides a global overview of the biogeographic traits of known bacterial genes involved in DMS/DMSP cycling from the Arctic and Antarctic oceans.Our study demonstrate that Puniceibacterium antarcticum SM1211 accumulates acrylate around cells through the degradation of DMSP via membrane-associated DddL,which offers protection against predation by the marine ciliate Uronema marinum.The research results are as follows:1.Biogeographic traits of DMS/DMSP cycling in polar oceansIn this chapter,we systematically investigated the biogeographic traits of 16 key microbial enzymes involved in DMS/DMSP cycling in metagenomic samples and metatranscriptomes from polar and non-polar datasets.Our analyses suggest that intense DMS/DMSP cycling occurs in the polar oceans.DMSP demethylase(DmdA),DMSP lyases(DddD,DddP and DddK)and trimethylamine monooxygenase(Tmm,which oxidizes DMS to dimethylsulfoxide)are the most prevalent bacterial genes involved in global DMS/DMSP cycling.Alphaproteobacteria(Pelagibacterales)and Gammaproteobacteria appear to play prominent roles in DMS/DMSP cycling in polar oceans.The microbial assemblages from the polar oceans are significantly correlated with water depth rather than geographic distance,suggesting that the differences of habitats between surface and deep waters rather than dispersal limitation are the key factors shaping microbial assemblages involved in DMS/DMSP cycling in polar oceans.2.The co-occurrence analyses of DMS/DMSP related enzymesTo uncover the co-occurrence of the genes in DMS/DMSP metabolism,we carried out a comprehensive co-occurrence network analysis of 214 microbial MAGs from polar oceans and all microbial genomes in the IMG/M database.Our results demonstrate that multiple DMS/DMSP cycling genes co-occurred in the same bacterial genome is a relatively common phenomenon.Strong co-existence clustering among various DMSP-degradation pathways is observed in both MAGs from polar oceans and microbial genomes from the IMG/M,suggesting that marine microbes likely employ multiple routes for DMSP catabolism.DMSP cleavage pathway and DMSP biosynthesis pathway show stronger connection in microbial genomes from the IMG/M than MAGs from polar oceans metagenomes.3.The acrylate accumulation mechanism in P.antarcticum SM1211P.antarcticum SM1211 was isolated from Antarctic waters,and contains a single dddL gene without any known acrylate-utilizing genes in its neighbourhood.Our study domenstrate that P.antarcticum SM1211 is unable to grow with DMSP or acrylate as the sole carbon source,but can produce and tolerate a high concentration of acrylate.Protein localization shows that DddL is a functional DMSP lyase and is membrane-associated.DddL is likely in the inner membrane with its catalytic domain facing the periplasm,enabling DMSP cleavage in the periplasm and acrylate release to the medium.The heterogeneous expressed DddL has relatively high catalytic efficiency and affinity compared to other DMSP lyases.4.Defense function of extracellular acrylate in P.antarcticum SM1211Previous reports show that the produced acrylate from DMSP cleavage can deter herbivores in DMSP-producing eukaryotic algae,however it is unclear if a parallel defense mechanism operates in marine bacteria.To test whether DMSP catabolism to acrylate plays a defensive role to protect P.antarcticum SM1211 against its predators,we investigated predator-prey interactions between this strain and U.marinum during both short-termmand long-term feeding experiments in the presence or absence of DMSP.The results indicate that when DMSP is present,acrylate produced from DMSP cleavage by P.antarcticum SM1211 via the membrane-associated DddL acts as a predation deterrent to U.marinum.The grazing protection provided by acrylate from DMSP cleavage by DddL shifts the predation preference and grazing pressure of U.marinum from strain SM1211 to non-dddL-containing bacteria.With this defense strategy,strain SM1211 not only gains a competitive advantage over other palatable strains in terms of nutrients and space,but also reduces its mortality.5.Universality of defense function of extracellular acrylateSearches showed that DddL homologues are widely distributed in saline waters,salt marshes,biofilms and marine symbionts,and also have an extensive dissemination potential.Our study shows that DddL-dependent grazer deterrent is not unique to P.antarcticum SM1211.This protection strategy enables other dddL-containing bacteria that do not use DMSP as carbon source to gain a survival advantage.Overall,by combining with metagenomic and metatranscriptomic analyses,our study provides a global overview of the biogeographic traits of known bacterial genes involved in DMS/DMSP cycling from the Arctic and Antarctic oceans and lays a solid foundation for further studies of DMS/DMSP cycling in polar ocean microbiome at the enzymatic,metabolic,and processual levels.Meanwhile,we show an inherent defense strategy performed by dddL-containing bacteria through conversion of DMSP into acrylate,which provides dddL-containing bacteria protection against grazing by protist predators.This protection strategy likely enable dddL-containing bacteria to gain a survival advantage,but moreover influences bacterial community structure and the flux of energy and matter across multi-trophic levels by shifting the predation pressure to non-dddL containing bacteria.This is a previously unrecognized bacterial chemical defense system with DMSP as the precursor compound,and shade light on elucidating the molecular mechanism of toxin production in chemically defended bacteria in the oceanic microecosystem.