Genome-resolved metagenomics revealed novel microbial taxa with ancient metabolism from macroscopic microbial mat structures inhabiting anoxic deep reefs of a Maldivian Blue Hole.
Journal
Environmental microbiology reports
ISSN: 1758-2229
Titre abrégé: Environ Microbiol Rep
Pays: United States
ID NLM: 101499207
Informations de publication
Date de publication:
Oct 2024
Oct 2024
Historique:
received:
22
03
2024
accepted:
12
07
2024
medline:
15
9
2024
pubmed:
15
9
2024
entrez:
13
9
2024
Statut:
ppublish
Résumé
Blue holes are vertical water-filled openings in carbonate rock that exhibit complex morphology, ecology, and water chemistry. In this study, macroscopic microbial mat structures found in complete anoxic conditions in the Faanu Mudugau Blue Hole (Maldives) were studied by metagenomic methods. Such communities have likely been evolutionary isolated from the surrounding marine environment for more than 10,000 years since the Blue Hole formation during the last Ice Age. A total of 48 high-quality metagenome-assembled genomes (MAGs) were recovered, predominantly composed of the phyla Chloroflexota, Proteobacteria and Desulfobacterota. None of these MAGs have been classified to species level (<95% ANI), suggesting the discovery of several new microbial taxa. In particular, MAGs belonging to novel bacterial genera within the order Dehalococcoidales accounted for 20% of the macroscopic mat community. Genome-resolved metabolic analysis of this dominant microbial fraction revealed a mixotrophic lifestyle based on energy conservation via fermentation, hydrogen metabolism and anaerobic CO
Identifiants
pubmed: 39267241
doi: 10.1111/1758-2229.13315
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13315Subventions
Organisme : Centro Nazionale di Ricerca - Biodiversità (Italy) project (PNRR CN00000033 - Centro Nazionale Biodiversità
ID : CN_00000033
Organisme : Italian Ministry of University and Research
ID : CUP D33C22000960007
Informations de copyright
© 2024 The Author(s). Environmental Microbiology Reports published by John Wiley & Sons Ltd.
Références
Adam, P.S., Borrel, G. & Gribaldo, S. (2018) Evolutionary history of carbon monoxide dehydrogenase/acetyl‐CoA synthase, one of the oldest enzymatic complexes. Proceedings of the National Academy of Sciences USA, 115, E1166–E1173.
Alneberg, J., Bjarnason, B.S., De Bruijn, I., Schirmer, M., Quick, J., Ijaz, U.Z. et al. (2014) Binning metagenomic contigs by coverage and composition. Nature Methods, 11, 1144–1146.
Azzola, A., Bianchi, C.N., Bianconi, G., Canganella, F., Doni, L., Montefalcone, M. et al. (2022) Microbial ecology across an oxic‐anoxic interface in a sulphidic blue hole. Memorie dell'Istituto Italiano di Speleologia S II, 42, 207–210.
Basen, M., Krüger, M., Milucka, J., Kuever, J., Kahnt, J., Grundmann, O. et al. (2011) Bacterial enzymes for dissimilatory sulfate reduction in a marine microbial mat (Black Sea) mediating anaerobic oxidation of methane. Environmental Microbiology, 13, 1370–1379.
Betzler, C., Lindhorst, S., Lüdmann, T., Weiss, B., Wunsch, M. & Braga, J.C. (2015) The leaking bucket of a Maldives atoll: implications for the understanding of carbonate platform drowning. Marine Geology, 366, 16–33.
Bianchi, C.N., Colantoni, P., Geister, J. & Morri, C. (1997) Reef geomorphology, sediments and ecological zonation at Felidu Atoll, Maldive Islands (Indian Ocean). In: Lessios, H.A. & MacIntyre, I.G. (Eds.) Proceedings of the 8th international coral reef symposium, Vol. 1. Panama: Smithsonian Tropical Research Institute, pp. 431–436.
Bianchi, C.N., Morri, C., Colantoni, P. & Sandrini, M. (2009) Italian research in the Maldives. Reef Encount 37: 17.
Björnerås, C., Škerlep, M., Gollnisch, R., Herzog, S.D., Ugge, G.E., Hegg, A. et al. (2020) Inland blue holes of The Bahamas – chemistry and biology in a unique aquatic environment. Fundamental and Applied Limnology, 194(2), 95–106.
Bolyen, E., Rideout, J.R., Dillon, M.R., Bokulich, N.A., Abnet, C.C., Al‐Ghalith, G.A. et al. (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology, 37, 852–857.
Bottrell, S.H., Smart, P.L., Whitaker, F. & Raiswell, R. (1991) Geochemistry and isotope systematics of sulphur in the mixing zone of Bahamian blue holes. Applied Geochemistry, 6, 97–103.
Callahan, B.J., Mcmurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.A. & Holmes, S.P. (2016) DADA2: high‐resolution sample inference from Illumina amplicon data. Nature Methods, 13(7), 581–583.
Canganella, F., Bianconi, G., Kato, C. & González, J. (2007) Microbial ecology of submerged marine caves and holes characterized by high levels of hydrogen sulphide. Reviews in Environmental Science and Biotechnology, 6, 61–70.
Chaumeil, P.A., Mussig, A.J., Hugenholtz, P. & Parks, D.H. (2020) GTDB‐Tk: a toolkit to classify genomes with the genome taxonomy database. Bioinformatics, 36, 1925–1927.
Chen, X., Liu, J., Zhu, X.‐Y., Xue, C.‐X., Yao, P., Fu, L. et al. (2023) Phylogenetically and metabolically diverse autotrophs in the world's deepest blue hole. ISME Communications, 3(1), 117.
Colantoni, P., Baldelli, G., Bianchi, C.N., Capaccioni, B., Morri, C., Sandrini, M. et al. (2003) A cave flooded by marine water with hydrogen sulphide highlights the recent evolution of the Maldives (Indian Ocean): preliminary notes. Grotte d'Italia s. V, 4, 29–37.
Cutroneo, L., Ahmed, H., Azzola, A., Fontana, H., Geneselli, I., Mancini, I. et al. (2023) First chemical–physical measurements by multi‐parameter probe in the blue hole of Faanu Mudugau (Ari Atoll, the Maldives). Environments, 10(10), 180.
Doni, L., Azzola, A., Bianchi, C.N., Bianconi, G., Canganella, F., Capello, M. et al. (2024) First characterization of the microbial communities of the blue hole of Faanu Mudugau, Maldives. Biologia Marina Mediterranea, 28(1), 1–4.
Droxler, A.W. & Jorry, S.J. (2021) The origin of modern atolls: challenging Darwin's deeply ingrained theory. Annual Review of Marine Science, 13, 537–573.
Fairbanks, R.G. (1989) A 17,000‐year glacio‐eustatic sea‐level record: influence of glacial melting rates on the younger Dryas event and deep‐ocean circulation. Nature, 342(6250), 637–642.
Gischler, E. (2011) Blue Hole. In: Finkl, C.W. (Ed.) Encyclopedia of earth sciences series. Dordrecht, Netherlands: Springer, pp. 164–165.
Gischler, E., Anselmetti, F.S. & Shinn, E.A. (2013) Seismic stratigraphy of the blue hole (lighthouse reef, Belize), a late Holocene climate and storm archive. Marine Geology, 344, 155–162.
Gischler, E., Shinn, E.A., Oschmann, W., Fiebig, J. & Buster, N.A. (2008) A 1500‐year Holocene Caribbean climate archive from the blue hole, lighthouse reef, Belize. Journal of Coastal Research, 24(6), 1495–1505.
Godfrey, T.J. (2018) Atlas of the Maldives, 6th edition. Australia: Atoll Editions; Cairns, p. 108.
Ho, T.Y., Taylor, G.T., Astor, Y., Varela, R., Müller‐Karger, F. & Scranton, M.I. (2004) Vertical and temporal variability of redox zonation in the water column of the Cariaco Basin: implications for organic carbon oxidation pathways. Marine Chemistry, 86, 89–104.
Hügler, M. & Sievert, S.M. (2011) Beyond the Calvin cycle: autotrophic carbon fixation in the ocean. Annual Review of Marine Science, 3, 261–289.
Jørgensen, B.B., Findlay, A.J. & Pellerin, A. (2019) The biogeochemical sulfur cycle of marine sediments. Frontiers in Microbiology, 10, 1–27.
Kang, D.D., Li, F., Kirton, E., Thomas, A., Egan, R., An, H. et al. (2019) MetaBAT 2: An adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ, 2019, 1–13.
Kindler, G.S., Wong, H.L., Larkum, A.W.D., Johnson, M., MacLeod, F.I. & Burns, B.P. (2022) Genome‐resolved metagenomics provides insights into the functional complexity of microbial mats in blue holes, Shark Bay. FEMS Microbiology Ecology, 98, 1–15.
Klostermann, L., Gischler, E., Storz, D. & Hudson, J.H. (2014) Sedimentary record of late Holocene event beds in a mid‐ocean atoll lagoon, Maldives, Indian Ocean: potential for deposition by tsunamis. Marine Geology, 348, 37–43.
Kovacs, S.E., van Hengstum, P.J., Reinhardt, E.G., Donnelly, J.P. & Albury, N.A. (2013) Late Holocene sedimentation and hydrologic development in a shallow coastal sinkhole on great Abaco Island, The Bahamas. Quaternary International, 317, 118–132.
Langerhans, R.B. (2017) Predictability and parallelism of multi trait adaptation. The Journal of Heredity, 109(1), 59–70.
Lee, M.D. (2019) GToTree: a user‐friendly workflow for phylogenomics. Bioinformatics, 35, 4162–4164.
Li, D., Liu, C.M., Luo, R., Sadakane, K. & Lam, T.W. (2015) MEGAHIT: An ultra‐fast single‐node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics, 31, 1674–1676.
Morri, C., Montefalcone, M., Lasagna, R., Gatti, G., Rovere, A., Parravicini, V. et al. (2015) Through bleaching and tsunami: coral reef recovery in the Maldives. Marine Pollution Bulletin, 98, 188–200.
Mushegian, A. (2008) Gene content of LUCA, the last universal common ancestor. Frontiers in Bioscience, 13(12), 4657–4666.
Mylroie, J.E., Carew, J.L. & Moore, A.I. (1995) Blue holes: definition and genesis. Carbonates and Evaporites, 10, 225–233.
Nguyen, L.T., Schmidt, H.A., Von Haeseler, A. & Minh, B.Q. (2015) IQ‐TREE: a fast and effective stochastic algorithm for estimating maximum‐likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274.
Olm, M.R., Brown, C.T., Brooks, B. & Banfield, J.F. (2017) DRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de‐replication. The ISME Journal, 11, 2864–2868.
Paerl, H.W., Pinckney, J.L. & Steppe, T.F. (2000) Cyanobacterial‐bacterial mat consortia: examining the functional unit of microbial survival and growth in extreme environments. Environmental Microbiology, 2, 11–26.
Parada, A.E., Needham, D.M. & Fuhrman, J.A. (2016) Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environmental Microbiology, 18, 1403–1414.
Parks, D.H., Imelfort, M., Skennerton, C.T., Hugenholtz, P. & Tyson, G.W. (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Research, 25(7), 1043–1055.
Patin, N.V., Dietrich, Z.A., Stancil, A., Quinan, M., Beckler, J.S., Hall, E.R. et al. (2021) Gulf of Mexico blue hole harbors high levels of novel microbial lineages. The ISME Journal, 15, 2206–2232.
Paulson, J. (2014) metagenomeSeq: statistical analysis for sparse high‐throughput sequencing. Bioconductor, 1, 191.
Pritchard, L., Glover, R.H., Humphris, S., Elphinstone, J.G. & Toth, I.K. (2016) Genomics and taxonomy in diagnostics for food security: soft‐rotting enterobacterial plant pathogens. Analytical Methods, 8, 12–24.
Purdy, E.G. & Bertram, G.T. (1993) Carbonate concepts from the Maldive, Indian Ocean. Studies in Geology, 34, 7–55.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P. et al. (2013) The SILVA ribosomal RNA gene database project: improved data processing and web‐based tools. Nucleic Acids Research, 41, 590–596.
Richter, M. & Rosselló‐Móra, R. (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proceedings of the National Academy of Sciences USA, 106, 19126–19131.
Rovere, A., Khanna, P., Bianchi, C.N., Droxler, A.W., Morri, C. & Naar, D.F. (2018) Submerged reef terraces in the Maldivian archipelago (Indian Ocean). Geomorphology, 317, 218–232.
Rufin‐Soler, C., Mörner, N.A., Laborel, J. & Collina‐Girard, J. (2014) Submarine morphology in the Maldives and Holocene sea‐level rise. Journal of Coastal Research, 30(1), 30–40.
Sandulli, R., Gallo D'Addabbo, M., Parisi, C., Pentassuglia, A. & de Zio Grimaldi, S. (2006) The meiofauna of Faanu Madugau blue hole, Ari atoll, Maldives. Biologia Marina Mediterranea, 13, 633–635.
Sandulli, R., Semprucci, F. & Balsamo, M. (2014) Taxonomic and functional biodiversity variations of meiobenthic and nematode assemblages across an extreme environment: a study case in a blue hole cave. International Journal of Zoology, 81(4), 508–516.
Santos, A., Bruna, P., Martinez‐Urtaza, J., Solís, F., Valenzuela, B., Zamorano, P. et al. (2021) Two archaeal metagenome‐assembled genomes from el tatio provide new insights into the crenarchaeota phylum. Genes, 12(3), 391.
Smith, A.R., Kieft, B., Mueller, R., Fisk, M.R., Mason, O.U., Popa, R. et al. (2019) Carbon fixation and energy metabolisms of a subseafloor olivine biofilm. The ISME Journal, 13, 1737–1749.
Smith, D.E., Harrison, S., Firth, C.R. & Jordan, J.T. (2011) The early Holocene sea level rise. Quaternary Science Reviews, 30(15–16), 1846–1860.
Song, D., Zhang, Y., Liu, J., Zhong, H., Zheng, Y., Zhou, S. et al. (2020) Metagenomic insights into the cycling of dimethylsulfoniopropionate and related molecules in the eastern China marginal seas. Frontiers in Microbiology, 11, 1–19.
Southward, A.J., Kennicut, M.C., II, Alcalà‐Herrera, J., Abbiati, M., Airoldi, L., Cinelli, F. et al. (1996) On the biology of submarine caves with sulphur springs: appraisal of 13C/12C ratios as a guide to trophic relations. Journal of the Marine Biological Association of the United Kingdom, 76(2), 265–285.
Sugio, T., Mizunashi, W., Inagaki, K. & Tano, T. (1987) Purification and some properties of sulfur:ferric ion oxidoreductase from Thiobacillus ferrooxidans. Journal of Bacteriology, 169, 4916–4922.
Sun, K., Yu, M., Zhu, X.‐Y., Xue, C.‐X., Zhang, Y., Chen, X. et al. (2023) Microbial communities related to the sulfur cycle in the Sansha Yongle blue hole. Microbiology Spectrum, 11(5), e01149‐2.
Uritskiy, G.V., DiRuggiero, J. & Taylor, J. (2018) MetaWRAP: a flexible pipeline for genome‐resolved metagenomic data analysis. Microbiome, 6, 1–13.
van Hengstum, P.J., Winkler, T.S., Tamalavage, A.E., Sullivan, R.M., Little, S.N., MacDonald, D. et al. (2020) Holocene sedimentation in a blue hole surrounded by carbonate tidal flats in The Bahamas: autogenic versus allogenic processes. Marine Geology, 419, 106051.
van Vliet, D.M., von Meijenfeldt, F.A.B., Dutilh, B.E., Villanueva, L., Sinninghe Damsté, J.S., Stams, A.J.M. et al. (2021) The bacterial sulfur cycle in expanding dysoxic and euxinic marine waters. Environmental Microbiology, 23, 2834–2857.
Weiss, M.C., Sousa, F.L., Mrnjavac, N., Neukirchen, S., Roettger, M., Nelson‐Sathi, S. et al. (2016) The physiology and habitat of the last universal common ancestor. Nature Microbiology, 1, 1–8.
Whitaker, F.F. & Smart, P.L. (1997) Groundwater circulation and geochemistry of a karstified bank‐marginal fracture system, South Andros Island, Bahamas. Journal of Hydrology, 197(1–4), 293–315.
Wong, H.L., MacLeod, F.I., White, R.A., Visscher, P.T. & Burns, B.P. (2020) Microbial dark matter filling the niche in hypersaline microbial mats. Microbiome, 8, 1–14.
Wu, Y.W., Simmons, B.A. & Singer, S.W. (2016) MaxBin 2.0: An automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics, 32, 605–607.
Wyrwoll, K.H., Zhu, R.Z., Collins, L.B. & Hatcher, B.G. (2006) Origin of blue hole structures in coral reefs: Houtman Abrolhos, Western Australia. Journal of Coastal Research, 22(1), 202–208.
Xie, L., Wang, B., Pu, X., Xin, M., He, P., Li, C. et al. (2019) Hydrochemical properties and chemocline of the Sansha Yongle blue hole in the South China Sea. Science of the Total Environment, 649, 1281–1292.
Yao, W. & Millero, F.J. (1993) The rate of sulfide oxidation by δMnO2 in seawater. Geochimica et Cosmochimica Acta, 57, 3359–3365.
Youssef, N.H., Farag, I.F., Rudy, S., Mulliner, A., Walker, K., Caldwell, F. et al. (2019) The Wood–Ljungdahl pathway as a key component of metabolic versatility in candidate phylum Bipolaricaulota (Acetothermia, OP1). Environmental Microbiology Reports, 11, 538–547.
Zhang, J.Z. & Millero, F.J. (1993) The products from the oxidation of H2S in seawater. Geochimica et Cosmochimica Acta, 57, 1705–1718.
Zhou, Z., Tran, P.Q., Breister, A.M., Liu, Y., Kieft, K., Cowley, E.S. et al. (2022) METABOLIC: high‐throughput profiling of microbial genomes for functional traits, metabolism, biogeochemistry, and community‐scale functional networks. Microbiome, 10, 1–22.
Zhuang, W.Q., Yi, S., Bill, M., Brisson, V.L., Feng, X., Men, Y. et al. (2014) Incomplete Wood–Ljungdahl pathway facilitates one‐carbon metabolism in organohalide‐respiring Dehalococcoides mccartyi. Proceedings of the National Academy of Sciences USA, 111, 6419–6424.