Phylogeny and biogeography of the algal DMS-releasing enzyme in the global ocean.
Journal
ISME communications
ISSN: 2730-6151
Titre abrégé: ISME Commun
Pays: England
ID NLM: 9918205372406676
Informations de publication
Date de publication:
14 Jul 2023
14 Jul 2023
Historique:
received:
21
02
2023
accepted:
29
06
2023
revised:
27
05
2023
medline:
15
7
2023
pubmed:
15
7
2023
entrez:
14
7
2023
Statut:
epublish
Résumé
Phytoplankton produce the volatile dimethyl sulfide (DMS), an important infochemical mediating microbial interactions, which is also emitted to the atmosphere and affecting the global climate. Albeit the enzymatic source for DMS in eukaryotes was elucidated, namely a DMSP lyase (DL) called Alma1, we still lack basic knowledge regarding its taxonomic distribution. We defined unique sequence motifs which enable the identification of DL homologs (DLHs) in model systems and environmental populations. We used these motifs to predict DLHs in diverse algae by analyzing hundreds of genomic and transcriptomic sequences from model systems under stress conditions and from environmental samples. Our findings show that the DL enzyme is more taxonomically widespread than previously thought, as it is encoded by known algal taxa as haptophytes and dinoflagellates, but also by chlorophytes, pelagophytes and diatoms, which were conventionally considered to lack the DL enzyme. By exploring the Tara Oceans database, we showed that DLHs are widespread across the oceans and are predominantly expressed by dinoflagellates. Certain dinoflagellate DLHs were differentially expressed between the euphotic and mesopelagic zones, suggesting a functional specialization and an involvement in the metabolic plasticity of mixotrophic dinoflagellates. In specific regions as the Southern Ocean, DLH expression by haptophytes and diatoms was correlated with environmental drivers such as nutrient availability. The expanded repertoire of putative DL enzymes from diverse microbial origins and geographic niches suggests new potential players in the marine sulfur cycle and provides a foundation to study the cellular function of the DL enzyme in marine microbes.
Identifiants
pubmed: 37452148
doi: 10.1038/s43705-023-00280-2
pii: 10.1038/s43705-023-00280-2
pmc: PMC10349084
doi:
Types de publication
Journal Article
Langues
eng
Pagination
72Subventions
Organisme : Israel Science Foundation (ISF)
ID : 1972/20
Informations de copyright
© 2023. The Author(s).
Références
Alcolombri U, Ben-Dor S, Feldmesser E, Levin Y, Tawfik DS, Vardi A. Identification of the algal dimethyl sulfide-releasing enzyme: a missing link in the marine sulfur cycle. Science. 2015;348:1466–9.
pubmed: 26113722
doi: 10.1126/science.aab1586
Hulswar S, Simó R, Galí M, Bell TG, Lana A, Inamdar S, et al. Third revision of the global surface seawater dimethyl sulfide climatology (DMS-Rev3). Earth Syst Sci Data. 2022;14:2963–87.
doi: 10.5194/essd-14-2963-2022
Simó R. Production of atmospheric sulfur by oceanic plankton: biogeochemical, ecological and evolutionary links. Trends Ecol Evol. 2001;16:287–94.
pubmed: 11369106
doi: 10.1016/S0169-5347(01)02152-8
Charlson RJ, Lovelock JE, Andreae MO, Warren SG. Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature. 1987;326:655–61.
doi: 10.1038/326655a0
Owen K, Saeki K, Warren J, Bocconcelli A, Wiley D, Ohira S-I, et al. Natural dimethyl sulfide gradients would lead marine predators to higher prey biomass. Commun Biol. 2021;4:149.
pubmed: 33526835
pmcid: 7851116
doi: 10.1038/s42003-021-01668-3
Shemi A, Alcolombri U, Schatz D, Farstey V, Vincent F, Rotkopf R, et al. Dimethyl sulfide mediates microbial predator–prey interactions between zooplankton and algae in the ocean. Nat Microbiol. 2021;6:1357–66.
pubmed: 34697459
doi: 10.1038/s41564-021-00971-3
Garcés E, Alacid E, Reñé A, Petrou K, Simó R. Host-released dimethylsulphide activates the dinoflagellate parasitoid Parvilucifera sinerae. ISME J. 2013;7:1065–8.
pubmed: 23344241
pmcid: 3635230
doi: 10.1038/ismej.2012.173
Foretich MA, Paris CB, Grosell M, Stieglitz JD, Benetti DD. Dimethyl sulfide is a chemical attractant for reef fish larvae. Sci Rep. 2017;7:2498.
pubmed: 28566681
pmcid: 5451384
doi: 10.1038/s41598-017-02675-3
Yoch DC. Dimethylsulfoniopropionate: its sources, role in the marine food web, and biological degradation to dimethylsulfide. Appl Environ Microbiol. 2002;68:5804–15.
pubmed: 12450799
pmcid: 134419
doi: 10.1128/AEM.68.12.5804-5815.2002
Caruana AMN, Malin G. The variability in DMSP content and DMSP lyase activity in marine dinoflagellates. Prog Oceanogr. 2014;120:410–24.
doi: 10.1016/j.pocean.2013.10.014
Bullock HA, Luo H, Whitman WB. Evolution of dimethylsulfoniopropionate metabolism in marine phytoplankton and bacteria. Front Microbiol. 2017;8:637.
pubmed: 28469605
pmcid: 5395565
doi: 10.3389/fmicb.2017.00637
Dougan KE, Deng Z-L, Wöhlbrand L, Reuse C, Bunk B, Chen Y, et al. Multi-omics analysis reveals the molecular response to heat stress in a “red tide” dinoflagellate. bioRxiv. 2022:2022.07.25.501386.
Naranjo-Ortíz MA, Brock M, Brunke S, Hube B, Marcet-Houben M, Gabaldón T. Widespread inter- and intra-domain horizontal gene transfer of d-amino acid metabolism enzymes in eukaryotes. Front Microbiol. 2016;7:2001.
Galí M, Devred E, Babin M, Levasseur M. Decadal increase in Arctic dimethylsulfide emission. Proc Natl Acad Sci USA. 2019;116:19311–17.
Park K, Kim I, Choi J-O, Lee Y, Jung J, Ha S-Y, et al. Unexpectedly high dimethyl sulfide concentration in high-latitude Arctic sea ice melt ponds. Environ Sci Process Impacts. 2019;21:1642–9.
pubmed: 31465050
doi: 10.1039/C9EM00195F
Vernette C, Lecubin J, Sánchez P, Coordinators TO, Sunagawa S, Delmont TO, et al. The Ocean Gene Atlas v2.0: online exploration of the biogeography and phylogeny of plankton genes. Nucleic Acids Res. 2022;50:W516–W26.
pubmed: 35687095
pmcid: 9252727
doi: 10.1093/nar/gkac420
Marchler-Bauer A, Bryant SH. CD-Search: protein domain annotations on the fly. Nucleic Acids Res. 2004;32:W327–31.
pubmed: 15215404
pmcid: 441592
doi: 10.1093/nar/gkh454
Bailey TL. STREME: accurate and versatile sequence motif discovery. Bioinformatics. 2021;37:2834–40.
pubmed: 33760053
pmcid: 8479671
doi: 10.1093/bioinformatics/btab203
Shinzato C, Khalturin K, Inoue J, Zayasu Y, Kanda M, Kawamitsu M, et al. Eighteen coral genomes reveal the evolutionary origin of Acropora strategies to accommodate environmental changes. Mol Biol Evol. 2020;38:16–30.
pmcid: 7783167
doi: 10.1093/molbev/msaa216
Chiu Y-L, Shinzato C. Evolutionary history of DMSP lyase-like genes in animals and their possible involvement in evolution of the scleractinian coral genus, Acropora. Front Mar Sci. 2022;9:889866.
Chan CX, Gross J, Yoon HS, Bhattacharya D. Plastid origin and evolution: new models provide insights into old problems. Plant Physiol. 2011;155:1552–60.
pubmed: 21343425
pmcid: 3091110
doi: 10.1104/pp.111.173500
De Clerck O, Kao SM, Bogaert KA, Blomme J, Foflonker F, Kwantes M, et al. Insights into the evolution of multicellularity from the sea lettuce genome. Curr Biol. 2018;28:2921–33.e5.
pubmed: 30220504
doi: 10.1016/j.cub.2018.08.015
de Souza MP, Chen YP, Yoch DC. Dimethylsulfoniopropionate lyase from the marine macroalga Ulva curvata: purification and characterization of the enzyme. Planta. 1996;199:433–8.
doi: 10.1007/BF00195736
Dickson DMJ, Kirst GO. The role of β-dimethylsulphoniopropionate, glycine betaine and homarine in the osmoacclimation of Platymonas subcordiformis. Planta. 1986;167:536–43.
pubmed: 24240370
doi: 10.1007/BF00391230
Gebser B, Thume K, Steinke M, Pohnert G. Phytoplankton-derived zwitterionic gonyol and dimethylsulfonioacetate interfere with microbial dimethylsulfoniopropionate sulfur cycling. MicrobiologyOpen. 2020;9:e1014.
pubmed: 32113191
pmcid: 7221440
doi: 10.1002/mbo3.1014
McParland EL, Wright A, Art K, He M, Levine NM. Evidence for contrasting roles of dimethylsulfoniopropionate production in Emiliania huxleyi and Thalassiosira oceanica. New Phytol. 2020;226:396–409.
pubmed: 31850524
pmcid: 7154784
doi: 10.1111/nph.16374
Johansson ON, Töpel M, Pinder MIM, Kourtchenko O, Blomberg A, Godhe A, et al. Skeletonema marinoi as a new genetic model for marine chain-forming diatoms. Sci Rep. 2019;9:5391.
pubmed: 30940823
pmcid: 6445071
doi: 10.1038/s41598-019-41085-5
Spielmeyer A, Pohnert G. Daytime, growth phase and nitrate availability dependent variations of dimethylsulfoniopropionate in batch cultures of the diatom Skeletonema marinoi. J Exp Mar Biol Ecol. 2012;413:121–30.
doi: 10.1016/j.jembe.2011.12.004
Osuna-Cruz CM, Bilcke G, Vancaester E, De Decker S, Bones AM, Winge P, et al. The Seminavis robusta genome provides insights into the evolutionary adaptations of benthic diatoms. Nat Commun. 2020;11:3320.
pubmed: 32620776
pmcid: 7335047
doi: 10.1038/s41467-020-17191-8
Keeling PJ, Burki F, Wilcox HM, Allam B, Allen EE, Amaral-Zettler LA, et al. The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLOS Biol. 2014;12:e1001889.
pubmed: 24959919
pmcid: 4068987
doi: 10.1371/journal.pbio.1001889
Steinke M, Malin G, Gibb SW, Burkill PH. Vertical and temporal variability of DMSP lyase activity in a coccolithophorid bloom in the northern North Sea. Deep-Sea Res PT II. 2002;49:3001–16.
doi: 10.1016/S0967-0645(02)00068-1
Steinke M, Malin G, Archer S, Burkill P, Liss P. DMS production in a coccolithophorid bloom: evidence for the importance of dinoflagellate DMSP lyases. Aquat Microb Ecol. 2002;26:259–70.
doi: 10.3354/ame026259
Carradec Q, Pelletier E, Da Silva C, Alberti A, Seeleuthner Y, Blanc-Mathieu R, et al. A global ocean atlas of eukaryotic genes. Nat Commun. 2018;9:373.
pubmed: 29371626
pmcid: 5785536
doi: 10.1038/s41467-017-02342-1
Schoemann V, Becquevort S, Stefels J, Rousseau V, Lancelot C. Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. J Sea Res. 2005;53:43–66.
doi: 10.1016/j.seares.2004.01.008
Kasamatsu N, Hirano T, Kudoh S, Odate T, Fukuchi M. Dimethylsulfoniopropionate production by psychrophilic diatom isolates. J Phycol. 2004;40:874–8.
doi: 10.1111/j.1529-8817.2004.03122.x
Gutierrez-Rodriguez A, Pillet L, Biard T, Said-Ahmad W, Amrani A, Simó R, et al. Dimethylated sulfur compounds in symbiotic protists: a potentially significant source for marine DMS(P). Limnol Oceanogr. 2017;62:1139–54.
doi: 10.1002/lno.10491
Jeong HJ, Yoo YD, Kim JS, Seong KA, Kang NS, Kim TH. Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci. 2010;45:65–91.
doi: 10.1007/s12601-010-0007-2
Cohen NR, McIlvin MR, Moran DM, Held NA, Saunders JK, Hawco NJ, et al. Dinoflagellates alter their carbon and nutrient metabolic strategies across environmental gradients in the central Pacific Ocean. Nat Microbiol. 2021;6:173–86.
pubmed: 33398100
doi: 10.1038/s41564-020-00814-7
Haas P. The liberation of methyl sulphide by seaweed. Biochem J. 1935;29:1297–9.
pubmed: 16745792
pmcid: 1266628
doi: 10.1042/bj0291297
Moustafa A, Beszteri B, Maier UG, Bowler C, Valentin K, Bhattacharya D. Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science. 2009;324:1724–6.
pubmed: 19556510
doi: 10.1126/science.1172983
Kirst GO. Osmotic adjustment in phytoplankton and macroalgae. In: Kiene RP, Visscher PT, Keller MD, Kirst GO, editors. Biological and environmental chemistry of DMSP and related sulfonium compounds. Boston, MA: Springer US; 1996. p. 121–9.
Sunda W, Kieber DJ, Kiene RP, Huntsman S. An antioxidant function for DMSP and DMS in marine algae. Nature. 2002;418:317–20.
pubmed: 12124622
doi: 10.1038/nature00851
Stefels J. Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J Sea Res. 2000;43:183–97.
doi: 10.1016/S1385-1101(00)00030-7
Archer SD, Ragni M, Webster R, Airs RL, Geider RJ. Dimethyl sulfoniopropionate and dimethyl sulfide production in response to photoinhibition in Emiliania huxleyi. Limnol Oceanogr. 2010;55:1579–89.
doi: 10.4319/lo.2010.55.4.1579
Darroch L, Lavoie M, Levasseur M, Laurion I, Sunda W, Michaud S, et al. Effect of short-term light- and UV-stress on DMSP, DMS, and DMSP lyase activity in Emiliania huxleyi. Aquat Microb Ecol. 2015;74:173–85.
doi: 10.3354/ame01735
Sunda WG, Hardison R, Kiene RP, Bucciarelli E, Harada H. The effect of nitrogen limitation on cellular DMSP and DMS release in marine phytoplankton: climate feedback implications. Aquat Sci. 2007;69:341–51.
doi: 10.1007/s00027-007-0887-0
Thume K, Gebser B, Chen L, Meyer N, Kieber DJ, Pohnert G. The metabolite dimethylsulfoxonium propionate extends the marine organosulfur cycle. Nature. 2018;563:412–5.
pubmed: 30429546
doi: 10.1038/s41586-018-0675-0
Moustafa A, Evans AN, Kulis DM, Hackett JD, Erdner DL, Anderson DM, et al. Transcriptome profiling of a toxic dinoflagellate reveals a gene-rich protist and a potential impact on gene expression due to bacterial presence. PLOS One. 2010;5:e9688.
pubmed: 20300646
pmcid: 2837391
doi: 10.1371/journal.pone.0009688
Seymour J, Simó R, Ahmed T, Stocker R. Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science. 2010;329:342–5.
pubmed: 20647471
doi: 10.1126/science.1188418
Bucciarelli E, Ridame C, Sunda WG, Dimier-Hugueney C, Cheize M, Belviso S. Increased intracellular concentrations of DMSP and DMSO in iron-limited oceanic phytoplankton Thalassiosira oceanica and Trichodesmium erythraeum. Limnol Oceanogr. 2013;58:1667–79.
doi: 10.4319/lo.2013.58.5.1667
Procter J, Hopkins FE, Fileman ES, Lindeque PK. Smells good enough to eat: Dimethyl sulfide (DMS) enhances copepod ingestion of microplastics. Mar Pollut Bull. 2019;138:1–6.
pubmed: 30660250
doi: 10.1016/j.marpolbul.2018.11.014
Steinke M, Wolfe GV, Kirst GO. Partial characterisation of dimethylsulfoniopropionate (DMSP) lyase isozymes in 6 strains of Emiliania huxleyi. Mar Ecol. 1998;175:215–25.
doi: 10.3354/meps175215
Stefels J, van Boekel WHM. Production of DMS from dissolved DMSP in axenic cultures of the marine phytoplankton species Phaeocystis sp. Mar Ecol Prog Ser. 1993;97:11–8.
doi: 10.3354/meps097011
Alcolombri U, Lei L, Meltzer D, Vardi A, Tawfik DS. Assigning the algal source of dimethylsulfide using a selective lyase inhibitor. ACS Chem Biol. 2017;12:41–6.
pubmed: 28103686
doi: 10.1021/acschembio.6b00844
Faktorová D, Nisbet RER, Fernández Robledo JA, Casacuberta E, Sudek L, Allen AE, et al. Genetic tool development in marine protists: emerging model organisms for experimental cell biology. Nat Methods. 2020;17:481–94.
pubmed: 32251396
pmcid: 7200600
doi: 10.1038/s41592-020-0796-x
Oertel W, Wichard T, Weissgerber A. Transformation of Ulva mutabilis (Chlorophyta) by vector plasmids integrating into the genome. J Phycol. 2015;51:963–79.
pubmed: 26986891
doi: 10.1111/jpy.12336
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–10.
pubmed: 2231712
doi: 10.1016/S0022-2836(05)80360-2
Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, et al. Highly accurate protein structure prediction with AlphaFold. Nature. 2021;596:583–9.
pubmed: 34265844
pmcid: 8371605
doi: 10.1038/s41586-021-03819-2
Varadi M, Anyango S, Deshpande M, Nair S, Natassia C, Yordanova G, et al. AlphaFold protein structure database: massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Res. 2021;50:D439–D44.
pmcid: 8728224
doi: 10.1093/nar/gkab1061
Nelson DR, Hazzouri KM, Lauersen KJ, Jaiswal A, Chaiboonchoe A, Mystikou A, et al. Large-scale genome sequencing reveals the driving forces of viruses in microalgal evolution. Cell Host Microbe. 2021;29:250–66.e8.
pubmed: 33434515
doi: 10.1016/j.chom.2020.12.005
Rutgers University, grant NPR. Red algal resources to promote integrative research in algal genomics. http://porphyra.rutgers.edu/ .
Przeworski M. Draft genome of the staghorn coral Acropora millepora. https://przeworskilab.com/data/ .
Feldmesser E, Rosenwasser S, Vardi A, Ben-Dor S. Improving transcriptome construction in non-model organisms: integrating manual and automated gene definition in Emiliania huxleyi. BMC Genom. 2014;15:148.
doi: 10.1186/1471-2164-15-148
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, et al. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23:2947–8.
pubmed: 17846036
doi: 10.1093/bioinformatics/btm404
Villar E, Vannier T, Vernette C, Lescot M, Cuenca M, Alexandre A, et al. The Ocean Gene Atlas: exploring the biogeography of plankton genes online. Nucleic Acids Res. 2018;46:W289–W95.
pubmed: 29788376
pmcid: 6030836
doi: 10.1093/nar/gky376
Savoca MS. Chemoattraction to dimethyl sulfide links the sulfur, iron, and carbon cycles in high-latitude oceans. Biogeochemistry. 2018;138:1–21.
doi: 10.1007/s10533-018-0433-2