Biodiversity, environmental drivers, and sustainability of the global deep-sea sponge microbiome.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
02 09 2022
02 09 2022
Historique:
received:
21
08
2021
accepted:
11
08
2022
entrez:
2
9
2022
pubmed:
3
9
2022
medline:
9
9
2022
Statut:
epublish
Résumé
In the deep ocean symbioses between microbes and invertebrates are emerging as key drivers of ecosystem health and services. We present a large-scale analysis of microbial diversity in deep-sea sponges (Porifera) from scales of sponge individuals to ocean basins, covering 52 locations, 1077 host individuals translating into 169 sponge species (including understudied glass sponges), and 469 reference samples, collected anew during 21 ship-based expeditions. We demonstrate the impacts of the sponge microbial abundance status, geographic distance, sponge phylogeny, and the physical-biogeochemical environment as drivers of microbiome composition, in descending order of relevance. Our study further discloses that fundamental concepts of sponge microbiology apply robustly to sponges from the deep-sea across distances of >10,000 km. Deep-sea sponge microbiomes are less complex, yet more heterogeneous, than their shallow-water counterparts. Our analysis underscores the uniqueness of each deep-sea sponge ground based on which we provide critical knowledge for conservation of these vulnerable ecosystems.
Identifiants
pubmed: 36056000
doi: 10.1038/s41467-022-32684-4
pii: 10.1038/s41467-022-32684-4
pmc: PMC9440067
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
5160Commentaires et corrections
Type : ErratumIn
Informations de copyright
© 2022. The Author(s).
Références
Hawkes, N. et al. Glass sponge grounds on the Scotian Shelf and their associated biodiversity. Mar. Ecol. Prog. Ser. 614, 91–109 (2019).
doi: 10.3354/meps12903
Paoli, C., Montefalcone, M., Morri, C., Vassallo, P. & Bianchi, C. N. Marine Animal Forests: The Ecology of Benthic Biodiversity Hotspots 1271–1312 (Springer, 2016).
Ospar Commission. Background document for deep-sea sponge aggregations. Biodivers. Ser. 88 https://qsr2010.ospar.org/media/assessments/Species/P00485_deep_sea_sponge_aggregations.pdf (2010).
FAO. Report and documentation of the expert consultation on deep-sea fisheries in the high seas. FAO Fisheries Report 838 https://www.fao.org/3/a1341e/a1341e.pdf (2006).
Maldonado, M. et al. Marine Animal Forests: The Ecology of Benthic Biodiversity Hotspots 1–39 (Springer, 2016).
De Goeij, J. M. et al. Surviving in a marine desert: The sponge loop retains resources within coral reefs. Science 342, 108–110 (2013).
pubmed: 24092742
doi: 10.1126/science.1241981
Zumberge, J. A. et al. Demosponge steroid biomarker 26-methylstigmastane provides evidence for Neoproterozoic animals. Nat. Ecol. Evol. 2, 1709–1714 (2018).
pubmed: 30323207
pmcid: 6589438
doi: 10.1038/s41559-018-0676-2
Turner, E. C. Possible poriferan body fossils in early Neoproterozoic microbial reefs. Nature 596, 87–91 (2021).
pubmed: 34321662
pmcid: 8338550
doi: 10.1038/s41586-021-03773-z
Thomas, T. et al. Diversity, structure and convergent evolution of the global sponge microbiome. Nat. Commun. 7, 11870 (2016).
pubmed: 27306690
pmcid: 4912640
doi: 10.1038/ncomms11870
Moitinho-Silva, L. et al. Predicting the HMA-LMA status in marine sponges by machine learning. Front. Microbiol. 8, 1–14 (2017).
doi: 10.3389/fmicb.2017.00752
Pita, L., Rix, L., Slaby, B. M., Franke, A. & Hentschel, U. The sponge holobiont in a changing ocean: From microbes to ecosystems. Microbiome 6, 46 (2018).
pubmed: 29523192
pmcid: 5845141
doi: 10.1186/s40168-018-0428-1
Lurgi, M., Thomas, T., Wemheuer, B., Webster, N. S. & Montoya, J. M. Modularity and predicted functions of the global sponge-microbiome network. Nat. Commun. 10, 1–12 (2019).
doi: 10.1038/s41467-019-08925-4
Cleary, D. F. R. et al. The sponge microbiome within the greater coral reef microbial metacommunity. Nat. Commun. 10, 1–12 (2019).
doi: 10.1038/s41467-019-09537-8
Jackson, S. A. et al. Archaea appear to dominate the microbiome of Inflatella pellicula deep sea sponges. PLoS One 8, 1–8 (2013).
doi: 10.1371/journal.pone.0084438
Kennedy, J. et al. Evidence of a putative deep sea specific microbiome in marine sponges. PLoS One 9, 1–13 (2014).
doi: 10.1371/journal.pone.0091092
Reveillaud, J. et al. Host-specificity among abundant and rare taxa in the sponge microbiome. ISME J. 8, 1198–1209 (2014).
pubmed: 24401862
pmcid: 4030224
doi: 10.1038/ismej.2013.227
Borchert, E. et al. A novel cold active esterase from a deep sea sponge Stelletta normani metagenomic library. Front. Mar. Sci. 4, 1–13 (2017).
doi: 10.3389/fmars.2017.00287
Morganti, T. M. et al. Giant sponge grounds of Central Arctic seamounts are associated with extinct seep life. Nat. Commun. 13, 1–15 (2022).
doi: 10.1038/s41467-022-28129-7
Steinert, G. et al. Compositional and quantitative insights into bacterial and archaeal communities of South Pacific deep-sea sponges (Demospongiae and Hexactinellida. Front. Microbiol. 11, 1–16 (2020).
doi: 10.3389/fmicb.2020.00716
Ramirez-Llodra, E. et al. Deep, diverse and definitely different: Unique attributes of the world’s largest ecosystem. Biogeosciences 7, 2851–2899 (2010).
doi: 10.5194/bg-7-2851-2010
Tian, R. M. et al. The deep-sea glass sponge Lophophysema eversa harbours potential symbionts responsible for the nutrient conversions of carbon, nitrogen, and sulfur. Environ. Microbiol. 18, 2481–2494 (2016).
pubmed: 26637128
doi: 10.1111/1462-2920.13161
Bayer, K. et al. Microbial strategies for survival in the glass sponge Vazella pourtalesii. mSystems 5, 1–20 (2020).
doi: 10.1128/mSystems.00473-20
Rusch, D. B. et al. The Sorcerer II Global Ocean Sampling expedition: Northwest Atlantic through eastern tropical Pacific. PLoS Biol. 5, 0398–0431 (2007).
doi: 10.1371/journal.pbio.0050077
Schloissnig, S. et al. Genomic variation landscape of the human gut microbiome. Nature 493, 45–50 (2013).
pubmed: 23222524
doi: 10.1038/nature11711
Bashiardes, S., Godneva, A., Elinav, E. & Segal, E. Towards utilization of the human genome and microbiome for personalized nutrition. Curr. Opin. Biotechnol. 51, 57–63 (2018).
pubmed: 29223004
doi: 10.1016/j.copbio.2017.11.013
Sieber, M. et al. Neutrality in the metaorganism. PLoS Biol. 17, 1–21 (2019).
doi: 10.1371/journal.pbio.3000298
Moitinho-Silva, L. et al. The sponge microbiome project. GigaScience 6, 1–7 (2017).
pubmed: 29020741
doi: 10.1093/gigascience/gix077
Deines, P., Hammerschmidt, K. & Bosch, T. C. G. Microbial species coexistence depends on the host environment. MBio 11, 1–13 (2020).
doi: 10.1128/mBio.00807-20
Easson, C. G. & Thacker, R. W. Phylogenetic signal in the community structure of host-specific microbiomes of tropical marine sponges. Front. Microbiol. 5, 1–11 (2014).
doi: 10.3389/fmicb.2014.00532
Busch, K. et al. On giant shoulders: How a seamount affects the microbial community composition of seawater and sponges. Biogeosciences 17, 3471–3486 (2020).
doi: 10.5194/bg-17-3471-2020
Bayer, K., Jahn, M. T., Slaby, B. M., Moitinho-Silva, L. & Hentschel, U. Marine sponges as Chloroflexi hot spots: Genomic insights and high-resolution visualization of an abundant and diverse symbiotic clade. mSystems 3, 1–19 (2018).
doi: 10.1128/mSystems.00150-18
Bienhold, C., Zinger, L., Boetius, A. & Ramette, A. Diversity and biogeography of bathyal and abyssal seafloor bacteria. PLoS One 11, 1–20 (2016).
doi: 10.1371/journal.pone.0148016
Zinger, L., Boetius, A. & Ramette, A. Bacterial taxa-area and distance–decay relationships in marine environments. Mol. Ecol. 23, 954–964 (2014).
pubmed: 24460915
pmcid: 4230465
doi: 10.1111/mec.12640
Maldonado, M., Ribes, M. & van Duyl, F. C. Nutrient fluxes through sponges. Biology, budgets, and ecological implications. Adv. Mar. Biol. 62, 113–182 (2012).
pubmed: 22664122
doi: 10.1016/B978-0-12-394283-8.00003-5
Roberts, E. M. et al. Oceanographic setting and short-timescale environmental variability at an Arctic seamount sponge ground. Deep Sea Res. Part I Oceanogr. Res. Pap. 138, 98–113 (2018).
Roberts, E. et al. Water masses constrain the distribution of deep-sea sponges in the North Atlantic Ocean and Nordic Seas. Mar. Ecol. Prog. Ser. 659, 75–96 (2021).
doi: 10.3354/meps13570
Ridgway, N. M. Temperature and salinity of sea water at the ocean floor in the New Zealand region. N. Zeal. J. Mar. Freshw. Res. 3, 57–72 (1969).
doi: 10.1080/00288330.1969.9515278
Loeng, H. Features of the physical oceanographic conditions of the Barents Sea. Polar Res. 10, 5–18 (1991).
doi: 10.3402/polar.v10i1.6723
Fahrbach, E., Rohardt, G. & Krause, G. The Antarctic coastal current in the southeastern Weddell Sea. Polar Biol. 12, 171–182 (1992).
doi: 10.1007/BF00238257
Freiwald, A., Hühnerbach, V., Lindberg, B., Wilson, J. B. & Campbell, J. The Sula Reef Complex, Norwegian shelf. Facies 47, 179–200 (2002).
doi: 10.1007/BF02667712
Lavin, L. et al. The Sea 933–1001 (Harvard University Press, 2004).
Hu, H., Liu, Q., Lin, X. & Liu, W. The South Pacific subtropical mode water in the Tasman Sea. J. Ocean Univ. China 6, 107–116 (2007).
doi: 10.1007/s11802-007-0107-5
Aksenov, Y., Bacon, S., Coward, A. C. & Holliday, N. P. Polar outflow from the Arctic Ocean: A high resolution model study. J. Mar. Syst. 83, 14–37 (2010).
doi: 10.1016/j.jmarsys.2010.06.007
Rüggeberg, A., Flögel, S., Dullo, W. C., Hissmann, K. & Freiwald, A. Water mass characteristics and sill dynamics in a subpolar cold-water coral reef setting at Stjernsund, northern Norway. Mar. Geol. 282, 5–12 (2011).
doi: 10.1016/j.margeo.2010.05.009
Buhl-Mortensen, L. et al. Seafloor Geomorphology as Benthic Habitat 703–715 (Elsevier, 2012).
Chiswell, S. M., Bostock, H. C., Sutton, P. J. H. & Williams, M. J. Physical oceanography of the deep seas around New Zealand: A review. N. Zeal. J. Mar. Freshw. Res. 49, 286–317 (2015).
doi: 10.1080/00288330.2014.992918
Dever, M., Hebert, D., Greenan, B. J. W., Sheng, J. & Smith, P. C. Hydrography and coastal circulation along the Halifax Line and the connections with the Gulf of St. Lawrence. Atmos.-Ocean 54, 199–217 (2016).
doi: 10.1080/07055900.2016.1189397
Storesund, J. E. et al. Linking bacterial community structure to advection and environmental impact along a coast-fjord gradient of the Sognefjord, western Norway. Prog. Oceanogr. 159, 13–30 (2017).
pubmed: 29225381
pmcid: 5713631
doi: 10.1016/j.pocean.2017.09.002
Lozupone, C. A. & Knight, R. Global patterns in bacterial diversity. Proc. Natl Acad. Sci. USA 104, 11436–11440 (2007).
pubmed: 17592124
pmcid: 2040916
doi: 10.1073/pnas.0611525104
Sunagawa, S. et al. Structure and function of the global ocean microbiome. Science 348, 1261359 (2015).
pubmed: 25999513
doi: 10.1126/science.1261359
Thompson, L. R. et al. A communal catalogue reveals Earth’s multiscale microbial diversity. Nature 551, 457–463 (2017).
pubmed: 29088705
pmcid: 6192678
doi: 10.1038/nature24621
Fan, L. et al. Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proc. Natl Acad. Sci. USA 109, 1878–1887 (2012).
doi: 10.1073/pnas.1203287109
Ribes, M. et al. Functional convergence of microbes associated with temperate marine sponges. Environ. Microbiol. 14, 1224–1239 (2012).
pubmed: 22335606
doi: 10.1111/j.1462-2920.2012.02701.x
Louca, S. et al. Function and functional redundancy in microbial systems. Nat. Ecol. Evol. 2, 936–943 (2018).
pubmed: 29662222
doi: 10.1038/s41559-018-0519-1
Moitinho-Silva, L. et al. Specificity and transcriptional activity of microbiota associated with low and high microbial abundance sponges from the Red Sea. Mol. Ecol. 23, 1348–1363 (2014).
pubmed: 23957633
doi: 10.1111/mec.12365
Oschlies, A. A committed fourfold increase in ocean oxygen loss. Nat. Commun. 12, 1–8 (2021).
doi: 10.1038/s41467-021-22584-4
Johnson, G. C. & Lyman, J. M. Warming trends increasingly dominate global ocean. Nat. Clim. Chang. 10, 757–761 (2020).
doi: 10.1038/s41558-020-0822-0
Helm, R. R. et al. Protect high seas biodiversity. Science 372, 1048–1049 (2021).
pubmed: 34083479
doi: 10.1126/science.abj0581
Cavicchioli, R. et al. Scientists’ warning to humanity: Microorganisms and climate change. Nat. Rev. Microbiol. 17, 569–586 (2019).
pubmed: 31213707
pmcid: 7136171
doi: 10.1038/s41579-019-0222-5
Busch, K., Hethke, A., Clefsen, I. & Hentschel, U. Wet lab SOP of the deep-sea sponge microbiome project. protocols.io. https://doi.org/10.17504/protocols.io.kxygxer1kv8j/v1 (2022).
Busch, K. 16S-AmpliconCorePipeline (v1.0.0). Zenodo. https://doi.org/10.5281/zenodo.6857851 (2022).
Muyzer, G., Waal, E. C. D. E. & Uitierlinden, A. G. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59, 1–6 (1993).
doi: 10.1128/aem.59.3.695-700.1993
Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl Acad. Sci. USA 108, 4516–4522 (2011).
pubmed: 20534432
doi: 10.1073/pnas.1000080107
Bolyen, E. et al. Reproducible, interactive, scalable, and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852–857 (2019).
pubmed: 31341288
pmcid: 7015180
doi: 10.1038/s41587-019-0209-9
Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).
pubmed: 27214047
pmcid: 4927377
doi: 10.1038/nmeth.3869
Quast, C. et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 41, 590–596 (2013).
doi: 10.1093/nar/gks1219
R Development Core Team. R: A language and environment for statistical computing. http://www.r-project.org (2008).
Eren, A. M. et al. Anvi’o: An advanced analysis and visualization platform for ‘omics data. PeerJ 3, e1319 (2015).
pubmed: 26500826
pmcid: 4614810
doi: 10.7717/peerj.1319
Pante, E. & Simon-Bouhet, B. marmap: A Package for importing, plotting and analyzing bathymetric and topographic data in R. PLoS One 8, 6–9 (2013).
doi: 10.1371/journal.pone.0073051
WoRMS Editorial Board. World Register of Marine Species. https://www.marinespecies.org (2020).
Gloeckner, V. et al. The HMA-LMA dichotomy revisited: An electron microscopical survey of 56 sponge species. Biol. Bull. 227, 78–88 (2014).
pubmed: 25216505
doi: 10.1086/BBLv227n1p78
Busch, K. & Hentschel, U. CTD profiles of the global Deep-sea Sponge Microbiome Project. PANGAEA. https://doi.org/10.1594/PANGAEA.923035 (2022).
Garcia, H. E. et al. World Ocean Atlas 2018. NOAA Atlas NESDIS 83 3 https://www.ncei.noaa.gov/products/world-ocean-atlas (2018).
Garcia, H. E. et al. World Ocean Atlas 2018. NOAA Atlas NESDIS 84 4 https://www.ncei.noaa.gov/products/world-ocean-atlas (2018).
Locarnini, R. A. et al. World Ocean Atlas 2018. NOAA Atlas NESDIS 81 1 https://www.ncei.noaa.gov/products/world-ocean-atlas (2018).
Zweng, M. M. et al. World Ocean Atlas 2018. NOAA Atlas NESDIS 82 2 https://www.ncei.noaa.gov/products/world-ocean-atlas (2018).
Olsen, A. et al. GLODAPv2.2019—an update of GLODAPv2. Earth Syst. Sci. Data 11, 1437–1461 (2019).
doi: 10.5194/essd-11-1437-2019
Olsen, A. et al. An updated version of the global interior ocean biogeochemical data product, GLODAPv2.2020. Earth Syst. Sci. Data 12, 3653–3678 (2020).
doi: 10.5194/essd-12-3653-2020
NASA Goddard Space Flight Center, Ocean Ecology Laboratory, Ocean Biology Processing Group. Moderate-resolution Imaging Spectroradiometer (MODIS) Aqua Particulate Inorganic Carbon Data. https://doi.org/10.5067/AQUA/MODIS/L3M/PIC/2018 (2018).
NASA Goddard Space Flight Center, Ocean Ecology Laboratory, Ocean Biology Processing Group. Moderate-resolution Imaging Spectroradiometer (MODIS) Aqua Particulate Organic Carbon Data. https://doi.org/10.5067/AQUA/MODIS/L3M/POC/2018 (2018).
NASA Goddard Space Flight Center, Ocean Ecology Laboratory, Ocean Biology Processing Group. Moderate-resolution Imaging Spectroradiometer (MODIS) Aqua Chlorophyll Data. https://doi.org/10.5067/AQUA/MODIS/L3M/CHL/2018 (2018).
Monterey, G. & Levitus, S. Seasonal variability of mixed layer depth for the world ocean. NOAA Atlas NESDIS 14 https://www.nodc.noaa.gov/ (1997).
NOAA National Geophysical Data Center. ETOPO1 1 Arc-Minute Global Relief Model. NOAA National Centers for Environmental Information. https://doi.org/10.7289/V5C8276M (2009).
Costello, M. J. et al. Marine biogeographic realms and species endemicity. Nat. Commun. 8, 1–9 (2017).
doi: 10.1038/s41467-017-01121-2
Busch, K. & Hentschel, U. Metadata and NCBI-Accession numbers of the global Deep-sea Sponge Microbiome Project. PANGAEA. https://doi.org/10.1594/PANGAEA.923033 (2022).
Busch, K. Basic Source Data: Biodiversity, environmental drivers, and sustainability of the global deep-sea sponge microbiome. Zenodo. https://doi.org/10.5281/zenodo.6896034 (2022).
Schmitt, S. et al. Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J. 6, 564–576 (2012).
pubmed: 21993395
doi: 10.1038/ismej.2011.116