Phylogenomic analysis of lipid biosynthetic genes of Archaea shed light on the ‘lipid divide’
Corresponding Author
Laura Villanueva
Department of Marine Microbiology and Biogeochemistry, NIOZ, Royal Netherlands Institute for Sea Research, and Utrecht University, P.O. Box 59, 1790 AB Den Burg, Texel, The Netherlands
For correspondence. E-mail [email protected]; Tel. +31 0222369428/550; Fax +31 0222319674.Search for more papers by this authorStefan Schouten
Department of Marine Microbiology and Biogeochemistry, NIOZ, Royal Netherlands Institute for Sea Research, and Utrecht University, P.O. Box 59, 1790 AB Den Burg, Texel, The Netherlands
Faculty of Geosciences, Utrecht University, P.O. Box 80.021, Utrecht, 3508 TA, The Netherlands
Search for more papers by this authorJaap S. Sinninghe Damsté
Department of Marine Microbiology and Biogeochemistry, NIOZ, Royal Netherlands Institute for Sea Research, and Utrecht University, P.O. Box 59, 1790 AB Den Burg, Texel, The Netherlands
Faculty of Geosciences, Utrecht University, P.O. Box 80.021, Utrecht, 3508 TA, The Netherlands
Search for more papers by this authorCorresponding Author
Laura Villanueva
Department of Marine Microbiology and Biogeochemistry, NIOZ, Royal Netherlands Institute for Sea Research, and Utrecht University, P.O. Box 59, 1790 AB Den Burg, Texel, The Netherlands
For correspondence. E-mail [email protected]; Tel. +31 0222369428/550; Fax +31 0222319674.Search for more papers by this authorStefan Schouten
Department of Marine Microbiology and Biogeochemistry, NIOZ, Royal Netherlands Institute for Sea Research, and Utrecht University, P.O. Box 59, 1790 AB Den Burg, Texel, The Netherlands
Faculty of Geosciences, Utrecht University, P.O. Box 80.021, Utrecht, 3508 TA, The Netherlands
Search for more papers by this authorJaap S. Sinninghe Damsté
Department of Marine Microbiology and Biogeochemistry, NIOZ, Royal Netherlands Institute for Sea Research, and Utrecht University, P.O. Box 59, 1790 AB Den Burg, Texel, The Netherlands
Faculty of Geosciences, Utrecht University, P.O. Box 80.021, Utrecht, 3508 TA, The Netherlands
Search for more papers by this authorSummary
The lipid membrane is one of the most characteristic traits distinguishing the three domains of life. Membrane lipids of Bacteria and Eukarya are composed of fatty acids linked to glycerol-3-phosphate (G3P) via ester bonds, while those of Archaea possess isoprene-based alkyl chains linked by ether linkages to glycerol-1-phosphate (G1P), resulting in the opposite stereochemistry of the glycerol phosphate backbone. This ‘lipid divide’ has raised questions on the evolution of microbial life since eukaryotes are thought to have evolved from the Archaea, requiring a radical change in membrane composition. Here, we searched for homologs of enzymes involved in membrane lipid and fatty acid synthesis in a wide variety of archaeal genomes and performed phylogenomic analyses. We found that two uncultured archaeal groups, i.e. marine euryarchaeota group II/III and ‘Lokiarchaeota’, recently discovered descendants of the archaeal ancestor leading to eukaryotes, lack the gene to synthesize G1P and, consequently, the capacity to synthesize archaeal membrane lipids. However, our analyses reveal their genetic capacity to synthesize G3P-based ‘chimeric lipids’ with either two ether-bound isoprenoidal chains or with an ester-bound fatty acid instead of an ether-bound isoprenoid. These archaea may reflect the ‘archaea-to-eukaryote’ membrane transition stage which have led to the current ‘lipid divide’.
Supporting Information
Additional Supporting Information may be found in the online version of this article at the publisher's web-site:
| Filename | Description |
|---|---|
| emi13361-sup-0001-suppinfo1.jpg66.9 KB | Fig. S1. Archaeal 16S rRNA gene-based phylogeny modified from Spang et al. (2015). TACK, Thaumarchaeota-Aigarchaeota-Crenarchaeota-Korarchaeota superphylum; Bathyarchaeota (Miscellaneous Crenarchaeota Group, MCG and group C3); DSAG, Deep-Sea Archaeal Group/Marine Benthic Group B (including ‘Lokiarchaeum’; Spang et al., 2015); MHVG, Marine Hydrothermal Vent Group; Euryarchaeota superphylum includes the uncultured group II (MGII) and group III (MGIII) euryarchaeota, among others. DPANN superphylum includes Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, among others (Castelle et al., 2015). |
| emi13361-sup-0002-suppinfo2.jpg6 MB | Fig. S2. Phylogenetic tree of geranylgeranylglyceryl phosphate (GGGP) synthase homologs in archaeal genomes. Tree was constructed using the maximum likelihood method and the LG model plus gamma distribution and invariant site (LG+G+I). The scale bar represents number of substitutions per site. The analysis included 364 positions in the final dataset. Branch support was calculated with the approximate likelihood ratio test (aLRT) and values ≥50% are indicated on the branches. This tree showed the previously reported divergence of GGGP synthases in two different clusters (cluster 1 including the Halobacteriales, Archaeoglobales and Methanomicrobiales, Fig. S2B; and cluster 2 including Thaumarchaeota, Crenarchaeota and GGGP synthases of the rest of euryarchaeotal orders; Fig. S2A; Boucher et al., 2004; Villanueva et al., 2014). The putative GGGP synthase annotated in the ‘Lokiarchaeum’ genome. This sequence is closely related to GGGP synthases of the Thermoplasmatales, including uncultured marine group II and III euryarchaeota (MGII/III). Fig. S2C indicates the phylogenetic position of the Thaumarchaeota single cell genomes within the tree. |
| emi13361-sup-0003-suppinfo3.jpg435.7 KB | Fig. S3. Phylogenetic tree of putative digeranylgeranylglyceryl phosphate (DGGGP) synthase homologs in archaeal genomes. This tree is based on the putative archaeal DGGGP synthase phylogenetic tree by Villanueva et al. (2014). Tree was constructed using the maximum likelihood method and the LG model plus gamma distribution and invariant site (LG+G+I). The scale bar represents number of amino acid substitutions per site. The analysis included 422 positions in the final dataset. Branch support was calculated with the approximate likelihood ratio test (aLRT) and values ≥50% are indicated on the branches. Fig. S3A indicates the phylogenetic relationship between the thaumarchaeotal prenyltransferases and the archaeal DGGGP synthase. Fig. S3B indicates the distribution of the putative DGGGP synthases in the different archaeal groups. The putative DGGGP synthase annotated in the ‘Lokiarchaeum’ genome (indicated in bold) was closely related to the DGGGP synthases of the euryarchaeaotal group Archaeoglobales. Putative DGGGP synthases annotated in the genomes of the uncultured marine group II and III euryarchaeota are not clustered with the rest of the putative DGGGP synthases. |
| emi13361-sup-0004-suppinfo4.xlsx161.8 KB | Table S1. Compilation of NCBI accession numbers of the enzymes included in Table 1 for the different archaeal genomes analyzed in this study. |
| emi13361-sup-0005-suppinfo5.docx15.9 KB | Table S2. Presence (√ in green) and absence (× in red) putative homologs of enzymes involved in the archaeal membrane lipid and fatty acid biosynthetic pathways in the ‘Lokiarchaeum’ genome (Spang et al., 2015) and NCBI accession numbers (see Figs. 1 and 5, and text for details). |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Abascal, F., Zardoya, R., and Posada, D. (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104–2105.
- Brochier-Armanet, C., Forterre, P., and Gribaldo, S. (2011) Phylogeny and evolution of the Archaea: one hundred genomes later. Curr Opin Microbiol 3: 274–281.
- Brown, C.T., Hug, L.A., Thomas, B.C., Sharon, I., Castelle, C.J., Singh, A., et al. (2015) Unusual biology across a group comprising more than 15% of domain Bacteria. Nature 523: 208–211.
- Castelle, C.J., Wrighton, K.C., Thomas, B.C., Hug, L.A., Brown, C.T., Wilkins, M.J., et al. (2015) Genomic expansion of domain archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. Curr Biol 25: 690–701.
- Deschamps, P., Zivanovic, Y., Moreira, D., Rodriguez-Valera, F., and López-García, P. (2014) Pangenome evidence for extensive interdomain horizontal transfer affecting lineage core and shell genes in uncultured planktonic thaumarchaeota and euryarchaeota. Genome Biol Evol 6: 1549–1563.
- Dibrova, D.V., Galperin, M.Y., and Mulkidjanian, A.Y. (2014) Phylogenomic reconstruction of archaeal fatty acid metabolism. Environ Microbiol 16: 907–918.
- Edgar, R.C. (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
- Fan, Q., Relini, A., Cassinadri, D., Gambacorta, A., and Gliozzi, A. (1995) Stability against temperature and external agents of vesicles composed of archael bolaform lipids and egg PC. Biochim Biophys Acta 1240: 83–88.
- Fisher, E., Almaguer, C., Holic, R., Griac, P., and Patton-Vogt, J. (2005) Glycerophosphocholine-dependent growth requires Gde1p (YPL110c) and Git1p in Saccharomyces cerevisiae. J Biol Chem 280: 36110–36117.
- Gattinger, A., Schloter, M., and Munch, J.C. (2002) Phospholipid etherlipid and phospholipid fatty acid fingerprints in selected euryarchaeotal monocultures for taxonomic profiling. FEMS Microbiol Lett 213: 133–139.
- Golding, G.B., and Gupta, R.S. (1995) Protein-based phylogenies support a chimeric origin for the eukaryotic genome. Mol Biol Evol 12: 1–6.
- Gray, M., and Doolittle, W.F (1982) Has the endosymbiont hypothesis being proven? Microbiol Rev 46: 1–42.
- Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307–321.
- Guldan, H., Sterner, R., and Babinger, P. (2008) Identification and characterization of a bacterial glycerol-1-phosphate dehydrogenase: Ni2+-dependent AraM from Bacillus subtilis. Biochem 47: 7376–7384.
- Guy, L., and Ettema, T.J. (2011) The archaeal 'TACK' superphylum and the origin of eukaryotes. Trends Microbiol 19: 580–587.
- Han, J.-S., and Ishikawa, K. (2005) Active site of Zn(2+)-dependent sn-glycerol-1-dehydrogenase from Aeropyrum pernix K1. Archaea 1: 311–317.
- Istivan, T.S., and Coloe, P.J. (2006) Phospholipase A in Gram-negative bacteria and its role in pathogenesis. Microbiology 152: 1263–1274.
- Iverson, V., Morris, R.M., Frazar, C.D., Berthiaume, C.T., Morales, R.L., and Armbrust, E.V. (2012) Untangling genomes from metagenomes: revealing an uncultured class of marine Euryarchaeota. Science 335: 587–590.
- Jahn, U., Summons, R., Sturt, H., Grosjean, E., and Huber, H. (2004) Composition of the lipids of Nanoarchaeum equitans and their origin from its host Ignicoccus sp. strain KIN4/I. Archiv Microbiol 182: 404–413.
- Jung, M.Y., Park, S.J., Kim, S.J., Kim, J.G., Sinninghe Damsté, J.S., Jeon, C.O., and Rhee, S.K. (2014) A mesophilic, autotrophic, ammonia-oxidizing archaeon of thaumarchaeal group I.1a cultivated from a deep oligotrophic soil horizon. Appl Environ Microbiol 80: 3645–3655.
- Kates, M. (1993) The biochemistry of Archaea (Archaebacteria). In Membrane Lipids of Archaea. D.J. Kushner and A.T. Matheson (eds). Amsterdam, The Netherlands: Elsevier Science Publishers B.V., pp. 261–295.
- Kates, M., Wassef, M.K., and Kushner, D.J. (1968) Radioisotopic studies on the biosynthesis of the glyceryl diether lipids of Halobacterium cutirubrum. Can J Biochem 46: 971–977.
- Koga, Y., and Morii, H. (2007) Biosynthesis of ether-type polar lipids in archaea and evolutionary considerations. Microbiol Mol Biol Rev 71: 97–120.
- Koga, Y., Kyuragi, T., Nishihara, M., and Sone, N. (1998) Did archaeal and bacterial cells arise independently from non-cellular precursors? A hypothesis stating that the advent of membrane phospholipid with enantiomeric glycerol phosphate backbones caused the separation of the two lines of descent. J Mol Evol 47: 631.
- Koga, Y., Sone, N., Noguchi, S., and Morii, H. (2003) Transfer of pro-R hydrogen from NADH to dihydroxyacetonephosphate by sn-glycerol-1-phosphate dehy- drogenase from the archaeon Methanothermobacter thermautotrophicus. Biosci Biotechnol Biochem 67: 1605–1608.
- Langworthy, T.A., Mayberry, W.R., and Smith, P.F. (1974) Long-chain glycerol diether and polyol dialkyl glycerol triether lipids of Sulfolobus acidocaldarius. J Bacteriol 119: 106–116.
- Larson, T.J., Ehrmann, M., and Boos, W. (1983) Periplasmic glycerophosphodiester phosphodiesterase of Escherichia coli, a new enzyme of the glp regulon. J Biol Chem 258: 5428–5432.
- Lebedeva, E.V., Hatzenpichler, R., Pelletier, E., Schuster, N., Hauzmayer, S., Bulaev, A., et al. (2013) Enrichment and genome sequence of the group I.1a ammonia-oxidizing Archaeon “Ca. Nitrosotenuis uzonensis” representing a clade globally distributed in thermal habitats. PLoS One 8: e80835.
- Liu, X.L., Summons, R.E., and Hinrichs, H.U. (2012) 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.
- Lloyd, K.G., Schreiber, D.G., Petersen, D.G., Kjeldsen, K.U., Lever, M.A., Steen, A.D., et al. (2013) Predominant archaea in marine sediments degrade detrital proteins. Nature 496: 215–218.
- Lombard, J., López-García, P., and Moreira, D. (2012a) The early evolution of lipid membranes and the three domains of life. Nat Rev Microbiol 10: 507–515.
- Lombard, J., López-García, P., and Moreira, D. (2012b) Phylogenomic investigation of phospholipid synthesis in archaea. Archaea 2012: 630910.
- López-García, P., Brochier, C., Moreira, D., and Rodríguez-Valera, F. (2004) Comparative analysis of a genome fragment of an uncultivated mesopelagic crenarchaeote reveals multiple horizontal gene transfers. Environ Microbiol 6: 19–34.
- López-García, P., Zivanovic, Y., Deschamps, P., and Moreira, D. (2015) Bacterial gene import and mesophilic adaptation in archaea. Nat Rev Microbiol 13: 447–456.
- Martijn, J., and Ettema, T.J.G. (2013) From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell. Biochem Soc Trans 41: 451–457.
- Martin, W., and Russell, M.J. (2003) On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Philos Trans R Soc Lond B Biol Sci 358: 59–83.
- Matsumi, R., Atomi, H., Driessen, A.J., and van der Oost, J. (2011) Isoprenoid biosynthesis in Archaea–biochemical and evolutionary implications. Res Microbiol 162: 39–52.
- Nelson-Sathi, S., Dagan, T., Janssen, A., Steel, M., McInerney, J.O., Deppenmeier, U., and Martin, W.F. Acquisition of 1,000 eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea. Proc Natl Acad Sci USA 109: 20537–20542.
- Nishihara, M., Yamazaki, T., Oshima, T., and Koga, Y. (1999) sn-Glycerol-1-phosphate-forming activities in archaea: separation of archaeal phospholipid biosynthesis and glycerol catabolism by glycerophosphate enantiomers. J Bacteriol 181: 1330–1333.
- Pereto, J., Lopez-Garcia, P., and Moreira, D. (2004) Ancestral lipid biosynthesis and early membrane evolution. Trends Biochem Sci 29: 469–477.
- Peterhoff, D., Beer, B., Rajendran, C., Kumpula, E.P., Kapetaniou, E., Guldan, H., et al. (2014) A comprehensive analysis of the geranylgeranylglyceryl phosphate synthase enzyme family identifies novel members and reveals mechanisms of substrate specificity and quaternary structure organization. Mol Microbiol 92: 885–899.
- Rütters, H., Sass, H., Cypionka, H., and Rullkotter, J. (2001) Monoalkylether phospholipids in the sulfate-reducing bacteria Desulfosarcina variabilis and Desulforhabdus amnigenus. Arch Microbiol 176: 435–442.
- Santelli, E., Schwarzenbacher, R., McMullan, D., Biorac, T., Brinen, L.S., Canaves, J.M. (2004) Crystal structure of a glycerophosphodiester phosphodiesterase (GDPD) from Thermotoga maritima (TM1621) at 1.60Å resolution. Proteins 56: 167–170.
- Santoro, A.E., Dupont, C.L., Richter, R.A., Craig, M.T., Carini, P., McIlvin, M.R., et al. (2015) Genomic and proteomic characterization of “Candidatus Nitrosopelagicus brevis”: an ammonia-oxidizing archaeon from the open ocean. Proc Natl Acad Sci USA 112: 1173–1178.
- Schouten, S., Hopmans, E.C., Pancost, R.D., and Damsté, J.S. (2000) 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.
- Shimada, H., and Yamagishi, A. (2011) Stability of heterochiral hybrid membrane made of bacterial sn-G3P lipids and archaeal sn-G1P lipids. Biochem 50: 4114–4120.
- Sinninghe Damsté, J.S., Strous, M., Rijpstra, W.I., Hopmans, E.C., Geenevasen, J.A., van Duin, A.C., et al. (2002) Linearly concatenated cyclobutane lipids form a dense bacterial membrane. Nature 419: 708–712.
- Sinninghe Damsté, J.S., Rijpstra, W.I., Hopmans, E.C., Schouten, S., Balk, M., and Stams, A.J. (2007) Structural characterization of diabolic acid-based tetraester, tetraether and mixed ether/ester, membrane-spanning lipids of bacteria from the order Thermotogales. Arch Microbiol. 188: 629–641.
- Sinninghe Damsté, J.S., Rijpstra, W.I., Hopmans, E.C., Weijers, J.W., Foesel, B.U., Overmann, J., and Dedysh, S.N. (2011) 13,16-Dimethyl octacosanedioic acid (iso-diabolic acid), a common membrane-spanning lipid of Acidobacteria subdivisions 1 and 3. Appl Environ Microbiol 77: 4147–4154.
- Sinninghe Damsté, J.S., Rijpstra, W.I., Hopmans, E.C., Foesel, B.U., Wüst, P.K., Overmann, J., et al. (2014) Ether- and ester-bound iso-diabolic acid and other lipids in members of acidobacteria subdivision 4. Appl Environ Microbiol 80: 5207–5218.
- Sojo, V., Pomiankowski, A., and Lane, N. (2014) A bioenergetic basis for membrane divergence in archaea and bacteria. PLoS Biol. 12: e1001926.
- Spang, A., Saw, J.H., Jørgensen, S.L., Zaremba-Niedzwiedzka, K., Martijn, J., Lind, A.E., et al. (2015) Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521: 173––179.
- Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725–2729.
- Tommassen, J., Eiglmeier, K., Cole, S.T., Overduin, P., Larson, T.J., and Boos, W. (1991) Characterization of two genes, glpQ and ugpQ, encoding glycerophosphoryl diester phosphodiesterases of Escherichia coli. Mol Gen Genet 226: 321–327.
- van der Rest, B., Boisson, A.M., Gout, E., Bligny, R., and Douce, R. (2002) Glycerophosphocholine metabolism in higher plant cells. Evidence of a new glyceryl-phosphodiester phosphodiesterase. Plant Physiol 130: 244–255.
- Villanueva, L., Schouten, S., and Sinninghe Damsté, J.S. (2014) A Re-evaluation of the Archaeal Membrane Lipid Biosynthetic Pathway. Nat Rev Microbiol 12: 438–448.
- Wächtershäuser, G. (2003) From pre-cells to Eukarya–a tale of two lipids. Mol Microbiol 47: 13–22.
- Waters, E., Hohn, M.J., Ahel, I., Graham, D.E., Adams, M.D., Barnstead, M., et al. (2003) The genome of Nanoarchaeum equitans: insights into early archaeal evolution and derived parasitism. Proc Natl Acad Sci USA 100: 12984–12988.
- Weijers, J.W., Schouten, S., Hopmans, E.C., Geenevasen, J.A., David, O.R., Coleman, J.M., et al. (2006) Membrane lipids of mesophilic anaerobic bacteria thriving in peats have typical archaeal traits. Environ Microbiol 8: 648–655.
- Williams, T.A., Foster, P.G., Nye, T.M.W., Cox, C.J., and Embley, T.M. (2012) A congruent phylogenomic signal places eukaryotes within the Archaea. Proc R Soc B 279: 4870–4879.
- Woese, C.R, and Fox, G.E. (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Nat Acad Sci USA 74: 5088–5090.
- Zhaxybayeva, O., Swithers, K.S., Lapierre, P., Fournier, G.P., Bickhart, D.M., DeBoy, R.T., Nelson, K.E., et al. (2009) On the chimeric nature, thermophilic origin, and phylogenetic placement of the Thermotogales. Proc Natl Acad Sci USA. 106: 5865–5870.
