Identification of a protein responsible for the synthesis of archaeal membrane-spanning GDGT lipids.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
22 03 2022
22 03 2022
Historique:
received:
08
12
2021
accepted:
07
03
2022
entrez:
23
3
2022
pubmed:
24
3
2022
medline:
13
4
2022
Statut:
epublish
Résumé
Glycerol dibiphytanyl glycerol tetraethers (GDGTs) are archaeal monolayer membrane lipids that can provide a competitive advantage in extreme environments. Here, we identify a radical SAM protein, tetraether synthase (Tes), that participates in the synthesis of GDGTs. Attempts to generate a tes-deleted mutant in Sulfolobus acidocaldarius were unsuccessful, suggesting that the gene is essential in this organism. Heterologous expression of tes homologues leads to production of GDGT and structurally related lipids in the methanogen Methanococcus maripaludis (which otherwise does not synthesize GDGTs and lacks a tes homolog, but produces a putative GDGT precursor, archaeol). Tes homologues are encoded in the genomes of many archaea, as well as in some bacteria, in which they might be involved in the synthesis of bacterial branched glycerol dialkyl glycerol tetraethers.
Identifiants
pubmed: 35318330
doi: 10.1038/s41467-022-29264-x
pii: 10.1038/s41467-022-29264-x
pmc: PMC8941075
doi:
Substances chimiques
Membrane Lipids
0
Glycerol
PDC6A3C0OX
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1545Informations de copyright
© 2022. The Author(s).
Références
Koga, Y. & Morii, H. Biosynthesis of ether-type polar lipids in archaea and evolutionary considerations. Microbiol. Mol. Biol. Rev. 71, 97–120 (2007).
pubmed: 17347520
pmcid: 1847378
doi: 10.1128/MMBR.00033-06
Valentine, D. L. Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat. Rev. Microbiol. 5, 316–323 (2007).
pubmed: 17334387
doi: 10.1038/nrmicro1619
Schouten, S., Hopmans, E. C. & Damsté, J. S. S. The organic geochemistry of glycerol dialkyl glycerol tetraether lipids: a review. Org. Geochem. 54, 19–61 (2013).
doi: 10.1016/j.orggeochem.2012.09.006
Yosuke, K. Thermal adaptation of the archaeal and bacterial lipid membranes. Archaea 2012, 789652 (2012).
Lai, D., Springstead, J. R. & Monbouquette, H. G. Effect of growth temperature on ether lipid biochemistry in Archaeoglobus fulgidus. Extremophiles 12, 271–278 (2008).
pubmed: 18157503
doi: 10.1007/s00792-007-0126-6
Sprott, G. D., Meloche, M. & Richards, J. C. Proportions of diether, macrocyclic diether, and tetraether lipids in Methanococcus jannaschii grown at different temperatures. J. Bacteriol. 173, 3907–3910 (1991).
pubmed: 2050642
pmcid: 208025
doi: 10.1128/jb.173.12.3907-3910.1991
Patel, G. B., Agnew, B. J., Deschatelets, L., Fleming, L. P. & Sprott, G. D. In vitro assessment of archaeosome stability for developing oral delivery systems. Int. J. Pharm. 194, 39–49 (2000).
pubmed: 10601683
doi: 10.1016/S0378-5173(99)00331-2
Mathai, J. C., Sprott, G. D. & Zeidel, M. L. Molecular mechanisms of water and solute transport across archaebacterial lipid membranes. J. Biol. Chem. 276, 27266–27271 (2001).
pubmed: 11373291
doi: 10.1074/jbc.M103265200
Elling, F. J. et al. Chemotaxonomic characterisation of the thaumarchaeal lipidome. Environ. Microbiol. 19, 2618–2700 (2017).
doi: 10.1111/1462-2920.13759
Jayme, F. B. et al. Influence of growth phase, pH, and temperature on the abundance and composition of tetraether lipids in the thermoacidophile Picrophilus torridus. Front. Microbiol. 7, 1–5 (2016).
Sara, J. et al. The effects of temperature and growth phase on the lipidomes of Sulfolobus islandicus and Sulfolobus tokodaii. Life 5, 1539–1566 (2015).
doi: 10.3390/life5031539
Elling, F. J., Konneke, M., Mussmann, M., Greve, A. & Hinrichs, K. U. Influence of temperature, pH, and salinity on membrane lipid composition and TEX
doi: 10.1016/j.gca.2015.09.004
Zhou, A., Weber, Y., Chiu, B. K., Elling, F. J. & Leavitt, W. D. Energy flux controls tetraether lipid cyclization in Sulfolobus acidocaldarius. Environ. Microbiol. 22, 343–353 (2020).
pubmed: 31696620
doi: 10.1111/1462-2920.14851
Pearson, A. & Ingalls, A. E. Assessing the use of archaeal lipids as marine environmental proxies. Annu. Rev. Earth Planet. Sci. 41, 359–384 (2013).
doi: 10.1146/annurev-earth-050212-123947
Schouten, S., Hopmans, E. C., Schefu, E. & Sinninghe-Damste, J. S. Distributional variations in marine crenarchaeotal membrane lipids: a new tool for reconstructing ancient sea water temperatures? Earth Planet. Sci. Lett. 204, 265–274 (2002).
doi: 10.1016/S0012-821X(02)00979-2
Jain & Samta. Biosynthesis of archaeal membrane ether lipids. Front. Microbiol. 5, 641 (2014).
pubmed: 25505460
pmcid: 4244643
doi: 10.3389/fmicb.2014.00641
Broderick, J. B., Duffus, B. R., Duschene, K. S. & Shepard, E. M. Radical S-adenosylmethionine enzymes. Chem. Rev. 114, 4229–4317 (2014).
pubmed: 24476342
pmcid: 4002137
doi: 10.1021/cr4004709
Zeng, Z., Liu, X. L., Wei, J. H., Summons, R. E. & Welander, P. V. Calditol-linked membrane lipids are required for acid tolerance in Sulfolobus acidocaldarius. Proc. Natl Acad. Sci. USA 115, 12932–12937 (2018).
pubmed: 30518563
pmcid: 6305003
doi: 10.1073/pnas.1814048115
Zeng, Z., Liu, X. L., Farley, K. R., Wei, J. H. & Welander, P. V. GDGT cyclization proteins identify the dominant archaeal sources of tetraether lipids in the ocean. Proc. Natl Acad. Sci. USA 116, 22505–22511 (2019).
pubmed: 31591189
pmcid: 6842593
doi: 10.1073/pnas.1909306116
Coffinet, S. et al. Evidence for enzymatic backbone methylation of the main membrane lipids in the archaeon Methanomassiliicoccus luminyensis. Appl. Environ. Microbiol. 88, e02154–21 (2021).
Fitz, W. & Arigoni, D. Biosynthesis of 15,16-dimethyltriacontanedioic acid (diabolic acid) from [16-
doi: 10.1039/c39920001533
Isobe, K. et al. Geranylgeranyl reductase and ferredoxin from Methanosarcina acetivorans are required for the synthesis of fully reduced archaeal membrane lipid in Escherichia coli Cells. J. Bacteriol. 196, 417–423 (2014).
pubmed: 24214941
pmcid: 3911245
doi: 10.1128/JB.00927-13
Xu, Q. et al. Insights into substrate specificity of geranylgeranyl reductases revealed by the structure of digeranylgeranylglycerophospholipid reductase, an essential enzyme in the biosynthesis of archaeal membrane lipids. J. Mol. Biol. 404, 403–417 (2010).
pubmed: 20869368
pmcid: 3008412
doi: 10.1016/j.jmb.2010.09.032
Quehenberger, J., Pittenauer, E., Allmaier, G. & Spadiut, O. The influence of the specific growth rate on the lipid composition of Sulfolobus acidocaldarius. Extremophiles 24, 413–420 (2020).
pubmed: 32200441
pmcid: 7174258
doi: 10.1007/s00792-020-01165-1
Koga, Y., Morii, H., Akagawa-Matsushita, M. & Ohga, M. Correlation of polar lipid composition with 16S rRNA phylogeny in Methanogens. Further analysis of lipid component parts. Biosci. Biotechnol. Biochem. 62, 230–236 (1998).
pubmed: 27388514
doi: 10.1271/bbb.62.230
Comita, P. B. & Gagosian, R. B. Membrane lipid from deep-sea hydrothermal vent methanogen: a new macrocyclic glycerol diether. Science 222, 1329–1331 (1983).
pubmed: 17773336
doi: 10.1126/science.222.4630.1329
Baumann, L. M. F. et al. Intact polar lipid and core lipid inventory of the hydrothermal vent methanogens Methanocaldococcus villosus and Methanothermococcus okinawensis. Org. Geochem. 126, 33–42 (2018).
doi: 10.1016/j.orggeochem.2018.10.006
Comita, P. B., Gagosian, R. B., Pang, H. & Costello, C. E. Structural elucidation of a unique macrocyclic membrane lipid from a new, extremely thermophilic, deep-sea hydrothermal vent archaebacterium, Methanococcus jannaschii. J. Biol. Chem. 259, 15234–15241 (1984).
pubmed: 6549008
doi: 10.1016/S0021-9258(17)42540-3
Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N. & Sternberg, M. J. N. P. The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10, 845–858 (2015).
pubmed: 25950237
pmcid: 5298202
doi: 10.1038/nprot.2015.053
Moller, S., Croning, M. & Apweiler, R. J. B. Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 17, 646–653 (2001).
pubmed: 11448883
doi: 10.1093/bioinformatics/17.7.646
Baker, B. J., Anda, V. D., Seitz, K. W., Dombrowski, N. & Lloyd, K. G. Diversity, ecology and evolution of Archaea. Nat. Microbiol. 5, 887–900 (2020).
pubmed: 32367054
doi: 10.1038/s41564-020-0715-z
Lincoln, S. A., Wai, B., Eppley, J. M., Church, M. J. & DeLong, E. F. Planktonic Euryarchaeota are a significant source of archaeal tetraether lipids in the ocean. Proc. Natl Acad. Sci. USA 111, 9858–9863 (2014).
pubmed: 24946804
pmcid: 4103328
doi: 10.1073/pnas.1409439111
Haro-Moreno, J. M., Rodriguez-Valera, F., López-García, P., Moreira, D. & Martin-Cuadrado, A. B. New insights into marine group III Euryarchaeota, from dark to light. ISME J. 11, 1102–1117 (2017).
pubmed: 28085158
pmcid: 5437922
doi: 10.1038/ismej.2016.188
Cui, H. L., Yang, X., Gao, X. & Xu, X. W. Halobellus clavatus gen. nov., sp. nov. and Halorientalis regularis gen. nov., sp. nov., two new members of the family Halobacteriaceae. Int. J. Syst. Evol. Microbiol. 61, 2682–2689 (2011).
pubmed: 21169458
doi: 10.1099/ijs.0.025841-0
Castelle, C. J. et al. Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations. Nat. Rev. Microbiol. 16, 629–645 (2018).
pubmed: 30181663
doi: 10.1038/s41579-018-0076-2
Jahn, U., Summons, R., Sturt, H., Grosjean, E. & Huber, H. Composition of the lipids of Nanoarchaeum equitans and their origin from its host Ignicoccus sp. strain KIN4/I. Arch. Microbiol. 182, 404–413 (2004).
pubmed: 15492905
doi: 10.1007/s00203-004-0725-x
Weijers, J., Schouten, S., Hopmans, E. C., Geenevasen, J. & Damsté, J. S. S. Membrane lipids of mesophilic anaerobic bacteria thriving in peats have typical archaeal traits. Environ. Microbiol. 8, 648–657 (2006).
pubmed: 16584476
doi: 10.1111/j.1462-2920.2005.00941.x
Damste, J. S. S., Hopmans, E. C., Pancost, R. D., Schouten, S. & Geenevasen, J. A. J. Newly discovered non-isoprenoid glycerol dialkyl glycerol tetraether lipids in sediments. Chem. Commun. 17, 1683–1684 (2000).
doi: 10.1039/b004517i
Peterse, F., Kim, J. H., Schouten, S., Kristensen, D. K. & Damste, J. Constraints on the application of the MBT/CBT palaeothermometer at high latitude environments (Svalbard, Norway). Org. Geochem. 40, 692–699 (2009).
doi: 10.1016/j.orggeochem.2009.03.004
Tierney, J. E. & Russell, J. M. Distributions of branched GDGTs in a tropical lake system: Implications for lacustrine application of the MBT/CBT paleoproxy. Org. Geochem. 40, 1032–1036 (2009).
doi: 10.1016/j.orggeochem.2009.04.014
Schouten, S., Hopmans, E. C., Pancost, R. D. & Damste, J. S. Widespread occurrence of structurally diverse tetraether membrane lipids: Evidence for the ubiquitous presence of low-temperature relatives of hyperthermophiles. Proc. Natl Acad. Sci. USA 97, 14421–14426 (2000).
pubmed: 11121044
pmcid: 18934
doi: 10.1073/pnas.97.26.14421
Sinninghe, D. et al. An overview of the occurrence of ether- and ester- linked iso-diabolic acid membrane lipids in microbial cultures of the Acidobacteria: Implications for brGDGT paleoproxies for temperature and pH. Org. Geochem. 124, 63–76 (2018).
doi: 10.1016/j.orggeochem.2018.07.006
Halamka, T. A. et al. Oxygen limitation can trigger the production of branched GDGTs in culture. Geochem. Perspect. Lett. 19, 36–39 (2021).
doi: 10.7185/geochemlet.2132
Eguchi, T., Nishimura, Y. & Kakinuma, K. Importance of the isopropylidene terminal of geranylgeranyl group for the formation of tetraether lipid in methanogenic archaea. Tetrahedron Lett. 44, 3275–3279 (2003).
doi: 10.1016/S0040-4039(03)00627-0
Nemoto, N., Shida, Y., Shimada, H., Oshima, T. & Yamagishi, A. Characterization of the precursor of tetraether lipid biosynthesis in the thermoacidophilic archaeon Thermoplasma acidophilum. Extremophiles 7, 235–243 (2003).
pubmed: 12768455
doi: 10.1007/s00792-003-0315-x
Ji, X., Li, Y., Jia, Y., Wei, D. & Qi, Z. Mechanistic insights into the radical S -adenosyl- l -methionine enzyme NosL from a substrate analogue and the shunt products. Angew. Chem. Int. Ed. 128, 3395–3398 (2016).
doi: 10.1002/ange.201509900
Eguchi, T., Takyo, H., Morita, M., Kakinuma, K. & Koga, Y. Unusual double-bond migration as a plausible key reaction in the biosynthesis of the isoprenoidal membrane lipids of methanogenic archaea. Chem. Commun. 1545–1546 (2000).
Pearson, A. Resolving a piece of the archaeal lipid puzzle. Proc. Natl Acad. Sci. USA 116, 22423–22425 (2019).
pubmed: 31628253
pmcid: 6842619
doi: 10.1073/pnas.1916583116
Yokoyama, K. & Lilla, E. A. C–C bond forming radical SAM enzymes involved in the construction of carbon skeletons of cofactors and natural products. Nat. Prod. Rep. 35, 660–694 (2018).
pubmed: 29633774
pmcid: 6051890
doi: 10.1039/C8NP00006A
Gräther, O. & Arigoni, D. Detection of regioisomeric macrocyclic tetraethers in the lipids of Methanobacterium thermoautotrophicum and other archaeal organisms. J. Chem. Soc. 4, 405–406 (1995).
Liu, X. L., Dar, B., Cb, B. & Res, C. Glycerol configurations of environmental GDGTs investigated using a selective sn 2 ether cleavage protocol. Org. Geochem. 128, 57–62 (2019).
doi: 10.1016/j.orggeochem.2018.12.003
Weijers, J., Schouten, S., Donker, J., Hopmans, E. C. & Damsté, J. S. S. Environmental controls on bacterial tetraether membrane lipid distribution in soils. Geochim. Cosmochim. Acta 71, 703–713 (2007).
doi: 10.1016/j.gca.2006.10.003
Diomande, S. E., Christophe, N. T., Guinebretiere, M. H., Broussolle, V. & Brillard, J. Role of fatty acids in Bacillus environmental adaptation. Front. Microbiol. 6, 813 (2015).
pubmed: 26300876
pmcid: 4525379
Walters, A. D., Smith, S. E. & Chong, J. Shuttle vector system for Methanococcus maripaludis with improved transformation efficiency. Appl. Environ. Microbiol. 77, 2549–2551 (2011).
pubmed: 21296937
pmcid: 3067461
doi: 10.1128/AEM.02919-10
Sarmiento, F., Leigh, J. A. & Whitman, W. B. Genetic systems for hydrogenotrophic methanogens. Methods Enzymol. 494, 43–73 (2011).
pubmed: 21402209
doi: 10.1016/B978-0-12-385112-3.00003-2
Michaela, W. et al. Versatile genetic tool box for the Crenarchaeote Sulfolobus acidocaldarius. Front. Microbiol. 3, 1–12 (2012).
Zhe, L., Jain, R., Smith, P., Fetchko, T. & Whitman, W. B. Engineering the autotroph Methanococcus maripaludis for geraniol production. ACS Synth. Biol. 5, 577–581 (2016).
doi: 10.1021/acssynbio.5b00267
Tumbula, D. L., Makula, R. A. & Whitman, W. B. Transformation of Methanococcus maripaludis and identification of a Pst I‐like restriction system. FEMS Microbiol. Lett. 121, 309–314 (1994).
doi: 10.1111/j.1574-6968.1994.tb07118.x
Huguet, C., Hopmans, E. C., Febo-Ayala, W., Thompson, D. H. & Schouten, S. An improved method to determine the absolute abundance of glycerol dibiphytanyl glycerol tetraether lipids. Org. Geochem. 37, 1036–1041 (2006).
doi: 10.1016/j.orggeochem.2006.05.008
Schouten, S., Huguet, C., Hopmans, E. C., Kienhuis, M. & Damsté, J. S. S. Analytical methodology for TEX
pubmed: 17311408
doi: 10.1021/ac062339v
Yang et al. The 6-methyl branched tetraethers significantly affect the performance of the methylation index (MBT’) in soils from an altitudinal transect at Mount Shennongjia. Org. Geochem. 82, 42–53 (2015).
doi: 10.1016/j.orggeochem.2015.02.003
Delong, E. F. et al. Dibiphytanyl ether lipids in nonthermophilic Crenarchaeotes. Appl. Environ. Microbiol. 64, 1133–1138 (1998).
pubmed: 9501451
pmcid: 106379
doi: 10.1128/AEM.64.3.1133-1138.1998
Liu, X. L., Summons, R. E. & Hinrichs, K. U. Extending the known range of glycerol ether lipids in the environment: structural assignments based on tandem mass spectral fragmentation patterns. Rapid Commun. Mass Spectrom. 26, 2295–2302 (2012).
pubmed: 22956321
doi: 10.1002/rcm.6355
Godzik, L. A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659 (2006).
pubmed: 16731699
doi: 10.1093/bioinformatics/btl158
Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).
pubmed: 15034147
pmcid: 390337
doi: 10.1093/nar/gkh340
Capella-Gutierrez, S., Silla-Martinez, J. M. & Gabaldon, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).
pubmed: 19505945
pmcid: 2712344
doi: 10.1093/bioinformatics/btp348
Alexandros, S. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
Ivica, L. & Peer, B. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 44, W242–W245 (2016).
Imachi, H., Nobu, M. K., Nakahara, N., Morono, Y. & Takai, K. Isolation of an archaeon at the prokaryote–eukaryote interface. Nature 577, 519–525 (2020).
pubmed: 31942073
pmcid: 7015854
doi: 10.1038/s41586-019-1916-6
Bale, N. J. et al. New insights into the polar lipid composition of extremely halo(alkali)philic Euryarchaea from hypersaline lakes. Front. Microbiol. 10, 377 (2019).
pubmed: 30930858
pmcid: 6423904
doi: 10.3389/fmicb.2019.00377
Meador, T. B. et al. Thermococcus kodakarensis modulates its polar membrane lipids and elemental composition according to growth stage and phosphate availability. Front. Microbiol. 5, 10 (2014).
pubmed: 24523718
pmcid: 3906577
doi: 10.3389/fmicb.2014.00010
Hug, L. A. et al. A new view of the tree of life. Nat. Microbiol. 1, 16048 (2016).
pubmed: 27572647
doi: 10.1038/nmicrobiol.2016.48
Rinke, C. et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431–437 (2013).
pubmed: 23851394
doi: 10.1038/nature12352