Review

Asgard archaea: Diversity, function, and evolutionary implications in a range of microbiomes

  • Received: 03 December 2018 Accepted: 25 January 2019 Published: 30 January 2019
  • Elucidating the diversity of the Archaea has many important ecological and evolutionary implications. The Asgard superphylum of the archaea, described recently from metagenomic data, has reignited the decades-old debate surrounding the topology of the tree of life. This review synthesizes recent findings through publicly available genomes and literature to describe the current ecological and evolutionary significance of the Asgard superphylum. Asgard archaea have been found in a diverse range of microbiomes across the globe, primarily from sedimentary environments. Within these environments, positive correlations between specific members of the Asgard archaea and Candidate Division TA06 bacteria have been observed, opening up the possibility of symbiotic interactions between the groupings. Asgard archaeal genomes encode functionally diverse metabolic pathways, including the Wood-Ljungdahl pathway as a carbon-fixation strategy, putative nucleotide salvaging pathways, and novel mechanisms of phototrophy including new rhodopsins. Asgard archaea also appear to be active in nitrogen cycling. Asgard archaea encode genes involved in both dissimilatory nitrate reduction and denitrification, and for the potential to use atmospheric nitrogen or nitrite as nitrogen sources. Asgard archaea also may be involved in the transformation of sulfur compounds, indicating a putative role in sulfur cycling. To date, all Asgard archaeal genomes identified were described as obligately anaerobic. The Asgard archaea also appear to have important evolutionary implications. The presence of eukaryotic signature proteins and the affiliation of Asgard archaea in phylogenetic analyses appears to support two-domain topologies of the tree of life with eukaryotes emerging from within the domain of archaea, as opposed to the eukaryotes being a separate domain of life. Thus far, Heimdallarchaeota appears as the closest archaeal relative of eukaryotes.

    Citation: Fraser MacLeod, Gareth S. Kindler, Hon Lun Wong, Ray Chen, Brendan P. Burns. Asgard archaea: Diversity, function, and evolutionary implications in a range of microbiomes[J]. AIMS Microbiology, 2019, 5(1): 48-61. doi: 10.3934/microbiol.2019.1.48

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  • Elucidating the diversity of the Archaea has many important ecological and evolutionary implications. The Asgard superphylum of the archaea, described recently from metagenomic data, has reignited the decades-old debate surrounding the topology of the tree of life. This review synthesizes recent findings through publicly available genomes and literature to describe the current ecological and evolutionary significance of the Asgard superphylum. Asgard archaea have been found in a diverse range of microbiomes across the globe, primarily from sedimentary environments. Within these environments, positive correlations between specific members of the Asgard archaea and Candidate Division TA06 bacteria have been observed, opening up the possibility of symbiotic interactions between the groupings. Asgard archaeal genomes encode functionally diverse metabolic pathways, including the Wood-Ljungdahl pathway as a carbon-fixation strategy, putative nucleotide salvaging pathways, and novel mechanisms of phototrophy including new rhodopsins. Asgard archaea also appear to be active in nitrogen cycling. Asgard archaea encode genes involved in both dissimilatory nitrate reduction and denitrification, and for the potential to use atmospheric nitrogen or nitrite as nitrogen sources. Asgard archaea also may be involved in the transformation of sulfur compounds, indicating a putative role in sulfur cycling. To date, all Asgard archaeal genomes identified were described as obligately anaerobic. The Asgard archaea also appear to have important evolutionary implications. The presence of eukaryotic signature proteins and the affiliation of Asgard archaea in phylogenetic analyses appears to support two-domain topologies of the tree of life with eukaryotes emerging from within the domain of archaea, as opposed to the eukaryotes being a separate domain of life. Thus far, Heimdallarchaeota appears as the closest archaeal relative of eukaryotes.


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    All authors declare no conflicts of interest in this paper.

    [1] DeLong EF (1992) Archaea in coastal marine environments. P Natl Acad Sci USA 89: 5685–5689. doi: 10.1073/pnas.89.12.5685
    [2] Karner MB, DeLong EF, Karl DM (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409: 507. doi: 10.1038/35054051
    [3] Bintrim SB, Donohue TJ, Handelsman J, et al. (1997) Molecular phylogeny of Archaea from soil. P Natl Acad Sci USA 94: 277–282. doi: 10.1073/pnas.94.1.277
    [4] Adam PS, Borrel G, Brochier-Armanet C, et al. (2017) The growing tree of Archaea: new perspectives on their diversity, evolution and ecology. ISME J 11: 2407. doi: 10.1038/ismej.2017.122
    [5] Spang A, Caceres EF, Ettema TJ (2017) Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life. Science 357: eaaf3883. doi: 10.1126/science.aaf3883
    [6] Spang A, Saw JH, Jørgensen SL, et al. (2015) Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521: 173–179. doi: 10.1038/nature14447
    [7] Dombrowski N, Teske AP, Baker BJ (2018) Expansive microbial metabolic versatility and biodiversity in dynamic Guaymas Basin hydrothermal sediments. Nature Comm 9: 4999. doi: 10.1038/s41467-018-07418-0
    [8] Zaremba-Niedzwiedzka K, Caceres EF, Saw JH, et al. (2017) Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541: 353–358. doi: 10.1038/nature21031
    [9] Wong HL, White RA, Visscher PT, et al. (2018) Disentangling the drivers of functional complexity at the metagenomic level in Shark Bay microbial mat microbiomes. ISME J 12: 2619. doi: 10.1038/s41396-018-0208-8
    [10] Narrowe AB, Spang A, Stairs CW, et al. (2018) Complex evolutionary history of translation Elongation Factor 2 and diphthamide biosynthesis in Archaea and parabasalids. Genome Biol Evol 10: 2380–2393. doi: 10.1093/gbe/evy154
    [11] Seitz KW, Lazar CS, Hinrichs KU, et al. (2016) Genomic reconstruction of a novel, deeply branched sediment archaeal phylum with pathways for acetogenesis and sulfur reduction. ISME J 10: 1696. doi: 10.1038/ismej.2015.233
    [12] Liu Y, Zhou Z, Pan J, et al. (2018) Comparative genomic inference suggests mixotrophic lifestyle for Thorarchaeota. ISME J 12: 1021.
    [13] Tully BJ, Graham ED, Heidelberg JF (2018) The reconstruction of 2,631 draft metagenome-assembled genomes from the global oceans. Sci Data 5: 170203. doi: 10.1038/sdata.2017.203
    [14] Pushkarev A, Inoue K, Larom S, et al. (2018) A distinct abundant group of microbial rhodopsins discovered using functional metagenomics. Nature: 558: 595–599. doi: 10.1038/s41586-018-0225-9
    [15] Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. P Natl Acad Sci USA 74: 5088–5090. doi: 10.1073/pnas.74.11.5088
    [16] Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. P Natl Acad Sci USA 87: 4576–4579. doi: 10.1073/pnas.87.12.4576
    [17] Iwabe N, Kuma K, Hasegawa M, et al. (1989) Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. P Natl Acad Sci USA 86: 9355–9359. doi: 10.1073/pnas.86.23.9355
    [18] Lake JA, Henderson E, Oakes M, et al. (1984) Eocytes: a new ribosome structure indicates a kingdom with a close relationship to eukaryotes. P Natl Acad Sci USA 81: 3786–3790. doi: 10.1073/pnas.81.12.3786
    [19] Rivera MC, Lake JA (1992) Evidence that eukaryotes and eocyte prokaryotes are immediate relatives. Science 257: 74–76. doi: 10.1126/science.1621096
    [20] Eme L, Spang A, Lombard J, et al. (2017) Archaea and the origin of eukaryotes. Nat Rev Microbiol 15: 711. doi: 10.1038/nrmicro.2017.133
    [21] Vetriani C, Jannasch HW, MacGregor BJ, et al. (1999) Population structure and phylogenetic characterization of marine benthic archaea in deep-sea sediments. Appl Environ Microb 65: 4375–4384.
    [22] Takai K, Horikoshi K (1999) Genetic diversity of archaea in deep-sea hydrothermal vent environments. Genetics 152: 1285–1297.
    [23] Inagaki F, Suzuki M, Takai K, et al. (2003) Microbial communities associated with geological horizons in coastal subseafloor sediments from the Sea of Okhotsk. Appl Environ Microb 69: 7224–7235. doi: 10.1128/AEM.69.12.7224-7235.2003
    [24] Jørgensen SL, Thorseth IH, Pedersen RB, et al. (2013) Quantitative and phylogenetic study of the Deep Sea Archaeal Group in sediments of the Arctic mid-ocean spreading ridge. Front Microbiol 4: 299.
    [25] Braga RM, Dourado MN, Araújo WL (2016) Microbial interactions: ecology in a molecular perspective. Braz J Microbiol 47: 86–98. doi: 10.1016/j.bjm.2016.10.005
    [26] Weiss S, Van Treuren W, Lozupone C, et al. (2016) Correlation detection strategies in microbial data sets vary widely in sensitivity and precision. ISME J 10: 1669. doi: 10.1038/ismej.2015.235
    [27] Saghaï A, Gutiérrez‐Preciado A, Deschamps P, et al. (2017) Unveiling microbial interactions in stratified mat communities from a warm saline shallow pond. Environ Microbiol 19: 2405–2421. doi: 10.1111/1462-2920.13754
    [28] Baker BJ, Lazar CS, Teske AP, et al. (2015) Genomic resolution of linkages in carbon, nitrogen, and sulfur cycling among widespread estuary sediment bacteria. Microbiome 3: 14. doi: 10.1186/s40168-015-0077-6
    [29] Sousa FL, Neukirchen S, Allen JF, et al. (2016) Lokiarchaeon is hydrogen dependent. Nat Microbiol 1: 16034. doi: 10.1038/nmicrobiol.2016.34
    [30] Sousa FL, Martin WF (2014) Biochemical fossils of the ancient transition from geoenergetics to bioenergetics in prokaryotic one carbon compound metabolism. BBA-Bioenergetics 1837: 964–981. doi: 10.1016/j.bbabio.2014.02.001
    [31] Borrel G, Adam PS, Gribaldo S (2016) Methanogenesis and the Wood-Ljungdahl pathway: an ancient, versatile, and fragile association. Genome Biol Evol 8: 1706–1711. doi: 10.1093/gbe/evw114
    [32] Kanehisa M, Sato Y, Morishima K (2016) BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 428: 726–731. doi: 10.1016/j.jmb.2015.11.006
    [33] Ragsdale SW, Pierce E (2008) Acetogenesis and the Wood-Ljungdahl pathway of CO2 fixation. BBA-Proteins Proteom 1784: 1873–1898. doi: 10.1016/j.bbapap.2008.08.012
    [34] Sato T, Atomi H, Imanaka T (2007) Archaeal type III RuBisCOs function in a pathway for AMP metabolism. Science 315: 1003–1006. doi: 10.1126/science.1135999
    [35] Aono R, Sato T, Yano A, et al. (2012) Enzymatic characterization of AMP phosphorylase and ribose-1, 5-bisphosphate isomerase functioning in an archaeal AMP metabolic pathway. J Bacteriol 194: 6847–6855. doi: 10.1128/JB.01335-12
    [36] Li R, Chai M, Qiu GY (2016) Distribution, fraction, and ecological assessment of heavy metals in sediment-plant system in Mangrove Forest, South China Sea. PLoS One 11: e0147308. doi: 10.1371/journal.pone.0147308
    [37] Oremland RS, Stolz JF, Hollibaugh JT (2004) The microbial arsenic cycle in Mono Lake, California. FEMS Microbiol Ecol 48: 15–27. doi: 10.1016/j.femsec.2003.12.016
    [38] Jackson CR, Dugas SL (2003) Phylogenetic analysis of bacterial and archaeal arsC gene sequences suggests an ancient, common origin for arsenate reductase. BMC Evol Biol 3: 18. doi: 10.1186/1471-2148-3-18
    [39] Da Cunha V, Gaia M, Gadelle D, et al. (2017) Lokiarchaea are close relatives of Euryarchaeota, not bridging the gap between prokaryotes and eukaryotes. PLoS Genet 13: e1006810. doi: 10.1371/journal.pgen.1006810
    [40] Spang A, Eme L, Saw JH, et al. (2018) Asgard archaea are the closest prokaryotic relatives of eukaryotes. PLoS Genet 14: e1007080. doi: 10.1371/journal.pgen.1007080
    [41] Klinger CM, Spang A, Dacks JB, et al. (2016) Tracing the archaeal origins of eukaryotic membrane-trafficking system building blocks. Mol Biol Evol 33: 1528–1541. doi: 10.1093/molbev/msw034
    [42] Xue B, Robinson RC (2013) Guardians of the actin monomer. Eur J Cell Biol 92: 316–332. doi: 10.1016/j.ejcb.2013.10.012
    [43] Akıl C, Robinson RC (2018) Genomes of Asgard archaea encode profilins that regulate actin. Nature 562: 439. doi: 10.1038/s41586-018-0548-6
    [44] Gunning PW, Ghoshdastider U, Whitaker S, et al. (2015) The evolution of compositionally and functionally distinct actin filaments. J Cell Sci 128: 2009–2019. doi: 10.1242/jcs.165563
    [45] Javaux EJ, Knoll AH, Walter MR (2001) Morphological and ecological complexity in early eukaryotic ecosystems. Nature 412: 66. doi: 10.1038/35083562
    [46] Parfrey LW, Lahr DJ, Knoll AH, et al. (2011) Estimating the timing of early eukaryotic diversification with multigene molecular clocks. P Natl Acad Sci USA 108: 13624–13629. doi: 10.1073/pnas.1110633108
    [47] Nunoura T, Takaki Y, Kakuta J, et al. (2010) Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group. Nucleic Acids Res 39: 3204–3223.
    [48] James RH, Caceres EF, Escasinas A, et al. (2017) Functional reconstruction of a eukaryotic-like E1/E2/(RING) E3 ubiquitylation cascade from an uncultured archaeon. Nature Comm 8: 1120. doi: 10.1038/s41467-017-01162-7
    [49] Stock T, Rother M (2009) Selenoproteins in Archaea and Gram-positive bacteria. BBA-Gen Subjects 1790: 1520–1532. doi: 10.1016/j.bbagen.2009.03.022
    [50] Yoshizawa S, Böck A (2009) The many levels of control on bacterial selenoprotein synthesis. BBA-Gen Subjects 1790: 1404–1414. doi: 10.1016/j.bbagen.2009.03.010
    [51] Labunskyy VM, Hatfield DL, Gladyshev VN (2014) Selenoproteins: molecular pathways and physiological roles. Physiol Rev 94: 739–777. doi: 10.1152/physrev.00039.2013
    [52] Mariotti M, Lobanov AV, Manta B, et al. (2016) Lokiarchaeota marks the transition between the archaeal and eukaryotic selenocysteine encoding systems. Mol Biol Evol 33: 2441–2453. doi: 10.1093/molbev/msw122
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