Prokaryotic communities of the French Polynesian sponge Dactylospongia metachromia display a site-specific and stable diversity during an aquaculture trial.

Biogeography Farming trials French Polynesia Holobiont Marine sponges Microbiome

Journal

Antonie van Leeuwenhoek
ISSN: 1572-9699
Titre abrégé: Antonie Van Leeuwenhoek
Pays: Netherlands
ID NLM: 0372625

Informations de publication

Date de publication:
11 Apr 2024
Historique:
received: 01 03 2024
accepted: 28 03 2024
medline: 11 4 2024
pubmed: 11 4 2024
entrez: 11 4 2024
Statut: epublish

Résumé

Dynamics of microbiomes through time are fundamental regarding survival and resilience of their hosts when facing environmental alterations. As for marine species with commercial applications, such as marine sponges, assessing the temporal change of prokaryotic communities allows us to better consider the adaptation of sponges to aquaculture designs. The present study aims to investigate the factors shaping the microbiome of the sponge Dactylospongia metachromia, in a context of aquaculture development in French Polynesia, Rangiroa, Tuamotu archipelago. A temporal approach targeting explants collected during farming trials revealed a relative high stability of the prokaryotic diversity, meanwhile a complementary biogeographical study confirmed a spatial specificity amongst samples at different longitudinal scales. Results from this additional spatial analysis confirmed that differences in prokaryotic communities might first be explained by environmental changes (mainly temperature and salinity), while no significant effect of the host phylogeny was observed. The core community of D. metachromia is thus characterized by a high spatiotemporal constancy, which is a good prospect for the sustainable exploitation of this species towards drug development. Indeed, a microbiome stability across locations and throughout the farming process, as evidenced by our results, should go against a negative influence of sponge translocation during in situ aquaculture.

Identifiants

pubmed: 38602593
doi: 10.1007/s10482-024-01962-0
pii: 10.1007/s10482-024-01962-0
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

65

Subventions

Organisme : Direction des Ressources Marines
ID : 08858/VP/DRMM
Organisme : Direction des Ressources Marines
ID : 08858/VP/DRMM
Organisme : Direction des Ressources Marines
ID : 08858/VP/DRMM
Organisme : Government of French Polynesia
ID : 3299/MTF
Organisme : Government of French Polynesia
ID : 3299/MTF
Organisme : Nederlandse Organisatie voor Wetenschappelijk Onderzoek
ID : 16.161.301
Organisme : Nederlandse Organisatie voor Wetenschappelijk Onderzoek
ID : 16.161.301

Informations de copyright

© 2024. The Author(s).

Références

Aguila-Ramírez RN, Hernández-Guerrero CJ, González-Acosta B et al (2014) Antifouling activity of symbiotic bacteria from sponge Aplysina gerardogreeni. Int Biodeterior Biodegradation 90:64–70. https://doi.org/10.1016/j.ibiod.2014.02.003
doi: 10.1016/j.ibiod.2014.02.003
Aminot A, Rey F  (2001) Chlorophyll a: determination by spectroscopic methods. ICES Techniques Marine Environ Sci 30:17. https://doi.org/10.25607/OBP-278
Astudillo-García C, Bell JJ, Webster NS et al (2017) Evaluating the core microbiota in complex communities: A systematic investigation. Environ Microbiol 19:1450–1462. https://doi.org/10.1111/1462-2920.13647
doi: 10.1111/1462-2920.13647 pubmed: 28078754
Astudillo-García C, Bell JJ, Montoya JM et al (2020) Assessing the strength and sensitivity of the core microbiota approach on a highly diverse sponge reef. Environ Microbiol 22:3985–3999. https://doi.org/10.1111/1462-2920.15185
doi: 10.1111/1462-2920.15185 pubmed: 32827171
Banker RMW, Lipovac J, Stachowicz JJ, Gold DA (2022) Sodium molybdate does not inhibit sulfate-reducing bacteria but increases shell growth in the Pacific oyster Magallana gigas. PLoS ONE 17:e0262939. https://doi.org/10.1371/journal.pone.0262939
doi: 10.1371/journal.pone.0262939 pubmed: 35139090 pmcid: 8827440
Baquiran JIP, Conaco C (2018) Sponge-microbe partnerships are stable under eutrophication pressure from mariculture. Mar Pollut Bull 136:125–134. https://doi.org/10.1016/j.marpolbul.2018.09.011
doi: 10.1016/j.marpolbul.2018.09.011 pubmed: 30509793
Batista D, Costa R, Carvalho AP et al (2018) Environmental conditions affect activity and associated microorganisms of marine sponges. Mar Environ Res 142:59–68. https://doi.org/10.1016/j.marenvres.2018.09.020
doi: 10.1016/j.marenvres.2018.09.020 pubmed: 30274716
Bayer K, Jahn MT, Slaby BM et al (2018) Marine Sponges as Chloroflexi Hot Spots: Genomic Insights and High-Resolution Visualization of an Abundant and Diverse Symbiotic Clade. Systems 3:00150–18. https://doi.org/10.1128/mSystems.00150-18
doi: 10.1128/mSystems.00150-18
Bell JJ (2008) The functional roles of marine sponges. Estuar Coast Shelf Sci 79:341–353. https://doi.org/10.1016/j.ecss.2008.05.002
doi: 10.1016/j.ecss.2008.05.002
Bibi F, Yasir M, Al-Sofyani A et al (2020) Antimicrobial activity of bacteria from marine sponge Suberea mollis and bioactive metabolites of Vibrio sp. EA348. Saudi J Biol Sci 27:1139–1147. https://doi.org/10.1016/j.sjbs.2020.02.002
doi: 10.1016/j.sjbs.2020.02.002 pubmed: 32256176 pmcid: 7105658
Bierwirth J, Mantas TP, Villechanoux J, Cerrano C (2022) Restoration of marine sponges—what can we learn from over a century of experimental cultivation? Water 14:1055. https://doi.org/10.3390/w14071055
doi: 10.3390/w14071055
Borcard D, Legendre P, Drapeau P (1992) Partialling out the Spatial Component of Ecological Variation. Ecology 73:1045–1055. https://doi.org/10.2307/1940179
doi: 10.2307/1940179
Brinkmann CM, Marker A, Kurtböke Dİ (2017) An Overview on Marine Sponge-Symbiotic Bacteria as Unexhausted Sources for Natural Product Discovery. Diversity 9:40. https://doi.org/10.3390/d9040040
doi: 10.3390/d9040040
Busch K, Slaby BM, Bach W et al (2022) Biodiversity, environmental drivers, and sustainability of the global deep-sea sponge microbiome. Nat Commun 13:5160. https://doi.org/10.1038/s41467-022-32684-4
doi: 10.1038/s41467-022-32684-4 pubmed: 36056000 pmcid: 9440067
Callahan BJ, McMurdie PJ, Rosen MJ et al (2016) DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869
doi: 10.1038/nmeth.3869 pubmed: 27214047 pmcid: 4927377
Callahan BJ, McMurdie PJ, Holmes SP (2017) Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J 11:2639–2643. https://doi.org/10.1038/ismej.2017.119
doi: 10.1038/ismej.2017.119 pubmed: 28731476 pmcid: 5702726
Callahan BJ, Sankaran K, Fukuyama JA et al. (2016b) Bioconductor workflow for microbiome data analysis: from raw reads to community analyses. F1000Research 5:1492 https://doi.org/10.12688/f1000research.8986.2
Campana S, Busch K, Hentschel U et al (2021) DNA-stable isotope probing (DNA-SIP) identifies marine sponge-associated bacteria actively utilizing dissolved organic matter (DOM). Environ Microbiol 23:4489–4504. https://doi.org/10.1111/1462-2920.15642
doi: 10.1111/1462-2920.15642 pubmed: 34159693 pmcid: 8453545
Campana S, Demey C, Busch K et al (2021) Marine sponges maintain stable bacterial communities between reef sites with different coral to algae cover ratios. FEMS Microbiol Ecol 97:fiab115. https://doi.org/10.1093/femsec/fiab115
doi: 10.1093/femsec/fiab115 pubmed: 34351429 pmcid: 8378938
Capon RJ, MacLeod JK (1987) Revision of the absolute stereochemistry of ilimaquinone. J Org Chem 52:5059–5060
doi: 10.1021/jo00231a051
Cárdenas CA, Bell JJ, Davy SK et al (2014) Influence of environmental variation on symbiotic bacterial communities of two temperate sponges. FEMS Microbiol Ecol 88:516–527. https://doi.org/10.1111/1574-6941.12317
doi: 10.1111/1574-6941.12317 pubmed: 24617641
Carte B, Rose CB, Faulkner DJ (1985) 5-Epi-Ilimaquinone, a metabolite of the sponge Fenestraspongia sp. J Org Chem 50:2785–2787
doi: 10.1021/jo00215a039
Chen ML, Becraft ED, Pachiadaki M et al (2020) Hiding in plain sight: The globally distributed bacterial candidate Phylum PAUC34f. Front Microbiol 11:376. https://doi.org/10.3389/fmicb.2020.00376
doi: 10.3389/fmicb.2020.00376 pubmed: 32226422 pmcid: 7081726
Chombard C, Boury-Esnault N, Tillier S (1998) Reassessment of homology of morphological characters in tetractinellid sponges based on molecular data. Syst Biol 47:351–366. https://doi.org/10.1080/106351598260761
doi: 10.1080/106351598260761 pubmed: 12066683
Cleary DFR, Polónia ARM, Reijnen BT et al (2020) Prokaryote communities inhabiting endemic and newly discovered sponges and octocorals from the Red Sea. Microb Ecol 80:103–119. https://doi.org/10.1007/s00248-019-01465-w
doi: 10.1007/s00248-019-01465-w pubmed: 31932882
Cleary DFR, Polónia ARM, Swierts T et al (2022) Spatial and environmental variables structure sponge symbiont communities. Mol Ecol 31:4932–4948. https://doi.org/10.1111/mec.16631
doi: 10.1111/mec.16631 pubmed: 35881675 pmcid: 9804187
Cleary DFR, Polónia ARM, de Voogd NJ (2018) Prokaryote composition and predicted metagenomic content of two Cinachyrella Morphospecies and water from West Papuan Marine Lakes. FEMS Microbiology Ecology 94. https://doi.org/10.1093/femsec/fix175
Daletos G, de Voogd NJ, Müller WEG et al (2014) Cytotoxic and protein kinase inhibiting nakijiquinones and nakijiquinols from the sponge Dactylospongia metachromia. J Nat Prod 77:218–226. https://doi.org/10.1021/np400633m
doi: 10.1021/np400633m pubmed: 24479418
Davis NM, Proctor DM, Holmes SP et al (2018) Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome 6:226. https://doi.org/10.1186/s40168-018-0605-2
doi: 10.1186/s40168-018-0605-2 pubmed: 30558668 pmcid: 6298009
De Caralt S, Sánchez-Fontenla J, Uriz MJ, Wijffels RH (2010) In situ aquaculture methods for Dysidea avara (Demospongiae, Porifera) in the northwestern mediterranean. Mar Drugs 8:1731–1742. https://doi.org/10.3390/md8061731
doi: 10.3390/md8061731 pubmed: 20631865 pmcid: 2901820
de Voogd NJ (2007) The mariculture potential of the Indonesian reef-dwelling sponge Callyspongia (Euplacella) biru: Growth, survival and bioactive compounds. Aquaculture 262:54–64. https://doi.org/10.1016/j.aquaculture.2006.09.028
doi: 10.1016/j.aquaculture.2006.09.028
de Goeij JM, Lesser MP, Pawlik JR (2017) Nutrient fluxes and ecological functions of coral reef sponges in a changing ocean. In: Carballo JL, Bell JJ (eds) Climate Change, Ocean Acidification and Sponges: Impacts Across Multiple Levels of Organization. Springer International Publishing, Cham, pp 373–410
doi: 10.1007/978-3-319-59008-0_8
Dray S, Dufour A-B (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20. https://doi.org/10.18637/jss.v022.i04
doi: 10.18637/jss.v022.i04
Duckworth A (2009) Farming sponges to supply bioactive metabolites and bath sponges: a review. Mar Biotechnol 11:669–679. https://doi.org/10.1007/s10126-009-9213-2
doi: 10.1007/s10126-009-9213-2
Duckworth A, Battershill C (2003) Sponge aquaculture for the production of biologically active metabolites: the influence of farming protocols and environment. Aquaculture 221:311–329. https://doi.org/10.1016/S0044-8486(03)00070-X
doi: 10.1016/S0044-8486(03)00070-X
Duckworth AR, Battershill CN (2003) Developing farming structures for production of biologically active sponge metabolites. Aquaculture 217:139–156. https://doi.org/10.1016/S0044-8486(02)00038-8
doi: 10.1016/S0044-8486(02)00038-8
Easson CG, Thacker RW (2014) Phylogenetic signal in the community structure of host-specific microbiomes of tropical marine sponges. Front Microbiol 5:532. https://doi.org/10.3389/fmicb.2014.00532
doi: 10.3389/fmicb.2014.00532 pubmed: 25368606 pmcid: 4201110
Easson CG, Chaves-Fonnegra A, Thacker RW, Lopez JV (2020) Host population genetics and biogeography structure the microbiome of the sponge Cliona delitrix. Ecol Evol 10:2007. https://doi.org/10.1002/ece3.6033
doi: 10.1002/ece3.6033 pubmed: 32128133 pmcid: 7042757
Ehrlich H, Worch H (2007) Sponges as natural composites: from biomimetic potential to development of new biomaterials. Porifera Res: Biodivers Innovat Sustain 217–223
Engelberts JP, Robbins SJ, de Goeij JM et al (2020) Characterization of a sponge microbiome using an integrative genome-centric approach. ISME J 14:1100–1110. https://doi.org/10.1038/s41396-020-0591-9
doi: 10.1038/s41396-020-0591-9 pubmed: 31992859 pmcid: 7174397
Erwin PM, Pita L, López-Legentil S, Turon X (2012) Stability of sponge-associated bacteria over large seasonal shifts in temperature and irradiance. Appl Environ Microbiol 78:7358–7368. https://doi.org/10.1128/AEM.02035-12
doi: 10.1128/AEM.02035-12 pubmed: 22885741 pmcid: 3457113
Erwin PM, Coma R, López-Sendino P et al (2015) Stable symbionts across the HMA-LMA dichotomy: low seasonal and interannual variation in sponge-associated bacteria from taxonomically diverse hosts. FEMS Microbiol Ecol 91:fiv115. https://doi.org/10.1093/femsec/fiv115
doi: 10.1093/femsec/fiv115 pubmed: 26405300
Gavriilidou A, Avcı B, Galani A et al (2023) Candidatus Nemesobacterales is a sponge-specific clade of the candidate phylum Desulfobacterota adapted to a symbiotic lifestyle. ISME J 17:1808–1818. https://doi.org/10.1038/s41396-023-01484-z
doi: 10.1038/s41396-023-01484-z pubmed: 37587369
Glasl B, Smith CE, Bourne DG, Webster NS (2018) Exploring the diversity-stability paradigm using sponge microbial communities. Sci Rep 8:8425. https://doi.org/10.1038/s41598-018-26641-9
doi: 10.1038/s41598-018-26641-9 pubmed: 29849034 pmcid: 5976656
Gloor GB, Macklaim JM, Pawlowsky-Glahn V, Egozcue JJ (2017) Microbiome datasets are compositional: and this is not optional. Front Microbiol 8:2224. https://doi.org/10.3389/fmicb.2017.02224
doi: 10.3389/fmicb.2017.02224 pubmed: 29187837 pmcid: 5695134
Graham ED, Tully BJ (2021) Marine Dadabacteria exhibit genome streamlining and phototrophy-driven niche partitioning. ISME J 15:1248–1256. https://doi.org/10.1038/s41396-020-00834-5
doi: 10.1038/s41396-020-00834-5 pubmed: 33230264
Hadas E, Shpigel M, Ilan M (2005) Sea ranching of the marine sponge Negombata magnifica (Demospongiae, Latrunculiidae) as a first step for latrunculin B mass production. Aquaculture 244:159–169. https://doi.org/10.1016/j.aquaculture.2004.11.052
doi: 10.1016/j.aquaculture.2004.11.052
Happel L, Rondon R, Font A et al (2022) Stability of the microbiome of the sponge Mycale (Oxymycale) acerata in the Western Antarctic Peninsula. Front Microbiol 13:827863. https://doi.org/10.3389/fmicb.2022.827863
doi: 10.3389/fmicb.2022.827863 pubmed: 35444618 pmcid: 9014287
Hardoim CCP, Ramaglia ACM, Lôbo-Hajdu G, Custódio MR (2021) Community composition and functional prediction of prokaryotes associated with sympatric sponge species of southwestern Atlantic coast. Sci Rep 11:9576. https://doi.org/10.1038/s41598-021-88288-3
doi: 10.1038/s41598-021-88288-3 pubmed: 33953214 pmcid: 8100286
Harvey AL, Edrada-Ebel R, Quinn RJ (2015) The re-emergence of natural products for drug discovery in the genomics era. Nat Rev Drug Discov 14:111–129. https://doi.org/10.1038/nrd4510
doi: 10.1038/nrd4510 pubmed: 25614221
Hentschel U, Hopke J, Horn M et al (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol 68:4431–4440. https://doi.org/10.1128/AEM.68.9.4431-4440.2002
doi: 10.1128/AEM.68.9.4431-4440.2002 pubmed: 12200297 pmcid: 124103
Hill M, Hill A, Lopez N, Harriott O (2006) Sponge-specific bacterial symbionts in the Caribbean sponge, Chondrilla nucula (Demospongiae, Chondrosida). Mar Biol 148:1221–1230. https://doi.org/10.1007/s00227-005-0164-5
doi: 10.1007/s00227-005-0164-5
Hitora Y, Sejiyama A, Honda K et al (2021) Fluorescent image-based high-content screening of extracts of natural resources for cell cycle inhibitors and identification of a new sesquiterpene quinone from the sponge. Dactylospongia metachromia Bioorg Med Chem 31:115968. https://doi.org/10.1016/j.bmc.2020.115968
doi: 10.1016/j.bmc.2020.115968 pubmed: 33387695
Hooper JNA, Van Soest RWM, Willenz P (eds) (2002) Systema Porifera. Springer, US, Boston, MA
Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP (2001) Bayesian Inference of Phylogeny and Its Impact on Evolutionary Biology. Science 294:2310–2314. https://doi.org/10.1126/science.1065889
doi: 10.1126/science.1065889 pubmed: 11743192
Hug LA, Thomas BC, Sharon I et al (2016) Critical biogeochemical functions in the subsurface are associated with bacteria from new phyla and little studied lineages. Environ Microbiol 18:159–173. https://doi.org/10.1111/1462-2920.12930
doi: 10.1111/1462-2920.12930 pubmed: 26033198
Hunting ER, Franken O, Knopperts F et al (2013) Substrate as a driver of sponge distributions in mangrove ecosystems. Mar Ecol Prog Ser 486:133–141. https://doi.org/10.3354/meps10376
doi: 10.3354/meps10376
Hutchins DA, Jansson JK, Remais JV et al (2019) Climate change microbiology — problems and perspectives. Nat Rev Microbiol 17:391–396. https://doi.org/10.1038/s41579-019-0178-5
doi: 10.1038/s41579-019-0178-5 pubmed: 31092905
Indraningrat AAG, Smidt H, Sipkema D (2016) Bioprospecting Sponge-Associated Microbes for Antimicrobial Compounds. Mar Drugs 14:87. https://doi.org/10.3390/md14050087
doi: 10.3390/md14050087 pubmed: 27144573 pmcid: 4882561
Jeong IH, Park J S (2013) Bacterial diversity of the South Pacific sponge, Dactylospongia metachromia based on DGGE fingerprinting. Korean J Microbiol 49(4)
Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066. https://doi.org/10.1093/nar/gkf436
doi: 10.1093/nar/gkf436 pubmed: 12136088 pmcid: 135756
Kochanowska AJ, Rao KV, Childress S et al (2008) Secondary metabolites from three Florida sponges with antidepressant activity. J Nat Prod 71:186–189. https://doi.org/10.1021/np070371u
doi: 10.1021/np070371u pubmed: 18217716 pmcid: 4918908
Lahti L, Shetty S, Blake T, Salojarvi J (2017) Tools for microbiome analysis in R. Version 1:28
Lamb CE, Watts JEM (2023) Microbiome species diversity and seasonal stability of two temperate marine sponges Hymeniacidon perlevis and Suberites massa. Environmental Microbiome 18:52. https://doi.org/10.1186/s40793-023-00508-7
doi: 10.1186/s40793-023-00508-7 pubmed: 37291644 pmcid: 10251714
Landwehr W, Wolf C, Wink J (2016) Actinobacteria and Myxobacteria-two of the most important bacterial resources for novel antibiotics. Curr Top Microbiol Immunol 398:273–302. https://doi.org/10.1007/82_2016_503
doi: 10.1007/82_2016_503 pubmed: 27704272
Leal CV, Avelino-Alves D, Salazar V et al (2022) Sponges present a core prokaryotic community stable across Tropical Western Atlantic. Sci Total Environ 835:155145. https://doi.org/10.1016/j.scitotenv.2022.155145
doi: 10.1016/j.scitotenv.2022.155145 pubmed: 35429557
Leary D, Vierros M, Hamon G et al (2009) Marine genetic resources: A review of scientific and commercial interest. Mar Policy 33:183–194. https://doi.org/10.1016/j.marpol.2008.05.010
doi: 10.1016/j.marpol.2008.05.010
Lemoine N, Buell N, Hill A, Hill M (2007) Assessing the utility of sponge microbial symbiont communities as models to study global climate change: a case study with Halichondria bowerbanki. Porifera Res: Biodiversity, Innovat Sustain 419–425
Lesser MP, Sabrina Pankey M, Slattery M et al (2022) Microbiome diversity and metabolic capacity determines the trophic ecology of the holobiont in Caribbean sponges. ISME COMMUN 2:1–12. https://doi.org/10.1038/s43705-022-00196-3
doi: 10.1038/s43705-022-00196-3
Lim SC, Putchakarn S, Thai MQ, Wang D, and Huang YM (2016) Inventory of sponge fauna from the Singapore Strait to Taiwan Strait along the western coastline of the South China Sea. Raffles Bulletin of Zoology
Lowe B, Venkatesan J, Ehrlich H, Kim SK (2016) Global constraints, prospects, and perspectives of marine sponge research. Marine Sponges: Chemicobiol Biomed Appl 25-35. https://doi.org/10.1007/978-81-322-2794-6_2
Lu P-H, Chueh S-C, Kung F-L et al (2007) Ilimaquinone, a marine sponge metabolite, displays anticancer activity via GADD153-mediated pathway. Eur J Pharmacol 556:45–54. https://doi.org/10.1016/j.ejphar.2006.10.061
doi: 10.1016/j.ejphar.2006.10.061 pubmed: 17140562
Maggioni F, Bell JJ, Pujo-Pay M et al (2023) Sponge organic matter recycling: Reduced detritus production under extreme environmental conditions. Mar Pollut Bull 190:114869. https://doi.org/10.1016/j.marpolbul.2023.114869
doi: 10.1016/j.marpolbul.2023.114869 pubmed: 37023545
Maggioni F, Stenger P-L, Jourand P, Majorel C (2023) The phylum Chloroflexi and their SAR202 clade dominate the microbiome of two marine sponges living in extreme environmental conditions. Mar Ecol 44:e12757. https://doi.org/10.1111/maec.12757
doi: 10.1111/maec.12757
Malve H (2016) Exploring the ocean for new drug developments: Marine pharmacology. J Pharm Bioallied Sci 8:83–91. https://doi.org/10.4103/0975-7406.171700
doi: 10.4103/0975-7406.171700 pubmed: 27134458 pmcid: 4832911
Maslin M (2022) Étude de la ressource en éponge Dactylospongia metachromia pour une production durable. Université de la Polynésie française, Theses
Maslin M, Gaertner-Mazouni N, Debitus C et al (2021) Marine sponge aquaculture towards drug development: An ongoing history of technical, ecological, chemical considerations and challenges. Aquaculture Reports 21:100813. https://doi.org/10.1016/j.aqrep.2021.100813
doi: 10.1016/j.aqrep.2021.100813
McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8:e61217. https://doi.org/10.1371/journal.pone.0061217
doi: 10.1371/journal.pone.0061217 pubmed: 23630581 pmcid: 3632530
McMurdie PJ, Holmes S (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol 10:e1003531. https://doi.org/10.1371/journal.pcbi.1003531
doi: 10.1371/journal.pcbi.1003531 pubmed: 24699258 pmcid: 3974642
Mehrshad M, Rodriguez-Valera F, Amoozegar MA et al (2018) The enigmatic SAR202 cluster up close: shedding light on a globally distributed dark ocean lineage involved in sulfur cycling. ISME J 12:655–668. https://doi.org/10.1038/s41396-017-0009-5
doi: 10.1038/s41396-017-0009-5 pubmed: 29208946
Meyer B, Kuever J (2008) Phylogenetic Diversity and Spatial Distribution of the Microbial Community Associated with the Caribbean Deep-water Sponge Polymastia cf. corticata by 16S rRNA, aprA, and amoA Gene Analysis. Microb Ecol 56:306–321. https://doi.org/10.1007/s00248-007-9348-5
doi: 10.1007/s00248-007-9348-5 pubmed: 18193317 pmcid: 2755779
Meyer CP, Geller JB, Paulay G (2005) Fine scale endemism on coral reefs: archipelagic differentiation in turbinid gastropods. Evolution 59:113–125
pubmed: 15792232
Mohamed NM, Enticknap JJ, Lohr JE et al (2008) Changes in bacterial communities of the marine sponge Mycale laxissima on transfer into aquaculture. Appl Environ Microbiol 74:1209–1222. https://doi.org/10.1128/AEM.02047-07
doi: 10.1128/AEM.02047-07 pubmed: 18156319
Mohamed NM, Rao V, Hamann MT et al (2008) Monitoring bacterial diversity of the marine sponge Ircinia strobilina upon transfer into aquaculture. Appl Environ Microbiol 74:4133–4143. https://doi.org/10.1128/AEM.00454-08
doi: 10.1128/AEM.00454-08 pubmed: 18469126 pmcid: 2446523
Moitinho-Silva L, Steinert G, Nielsen S et al (2017) Predicting the HMA-LMA status in marine sponges by machine learning. Front Microbiol 8:752. https://doi.org/10.3389/fmicb.2017.00752
doi: 10.3389/fmicb.2017.00752 pubmed: 28533766 pmcid: 5421222
Monteiro LCP (2020) Rhizospheric microbial communities of plants coexisting under different edaphic conditions. (Doctoral dissertation, Universidade Federal de Viçosa)
Morganti TM, Slaby BM, de Kluijver A et al (2022) Giant sponge grounds of Central Arctic seamounts are associated with extinct seep life. Nat Commun 13:638. https://doi.org/10.1038/s41467-022-28129-7
doi: 10.1038/s41467-022-28129-7 pubmed: 35136058 pmcid: 8826442
Morrow KM, Fiore CL, Lesser MP (2016) Environmental drivers of microbial community shifts in the giant barrel sponge, Xestospongia muta, over a shallow to mesophotic depth gradient. Environ Microbiol 18:2025–2038. https://doi.org/10.1111/1462-2920.13226
doi: 10.1111/1462-2920.13226 pubmed: 26769079
Neu AT, Allen EE, Roy K (2021a) Defining and quantifying the core microbiome: Challenges and prospects. Proc Natl Acad Sci 118:e2104429118. https://doi.org/10.1073/pnas.2104429118
doi: 10.1073/pnas.2104429118 pubmed: 34862327 pmcid: 8713806
Neu AT, Torchin ME, Allen EE & Roy K (2021b) Microbiome divergence of marine gastropod species separated by the Isthmus of Panama. bioRxiv. https://doi.org/10.1101/2021.07.08.451645
O’Brien PA, Tan S, Yang C et al (2020) Diverse coral reef invertebrates exhibit patterns of phylosymbiosis. ISME J 14:2211–2222. https://doi.org/10.1038/s41396-020-0671-x
doi: 10.1038/s41396-020-0671-x pubmed: 32444811 pmcid: 7608455
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara RB et al (2013) Community ecology package. R package version 2(0):321–326
Osinga R, Sidri M, Cerig E, Gokalp SZ, Gokalp M (2010) Sponge aquaculture trials in the East-Mediterranean Sea: new approaches to earlier ideas. The Open Marine Biol J 4(1). https://doi.org/10.2174/1874450801004010074
Pantile R, Webster N (2011) Strict thermal threshold identified by quantitative PCR in the sponge Rhopaloeides odorabile. Mar Ecol Prog Ser 431:97–105. https://doi.org/10.3354/meps09128
doi: 10.3354/meps09128
Parada AE, Needham DM, Fuhrman JA (2016) Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol 18:1403–1414. https://doi.org/10.1111/1462-2920.13023
doi: 10.1111/1462-2920.13023 pubmed: 26271760
Pawlik JR, McMurray SE (2020) The emerging ecological and biogeochemical importance of sponges on coral reefs. Ann Rev Mar Sci 12:315–337. https://doi.org/10.1146/annurev-marine-010419-010807
doi: 10.1146/annurev-marine-010419-010807 pubmed: 31226028
Pereira DM, Valentão P, Andrade PB (2013) Lessons from the Sea: Distribution, SAR, and molecular mechanisms of anti-inflammatory drugs from marine organisms. Stud Natur Prod Chem 40:205–228. https://doi.org/10.1016/B978-0-444-59603-1.00007-2
doi: 10.1016/B978-0-444-59603-1.00007-2
Piel J, Hui D, Wen G et al (2004) Antitumor polyketide biosynthesis by an uncultivated bacterial symbiont of the marine sponge Theonella swinhoei. Proc Natl Acad Sci 101:16222–16227. https://doi.org/10.1073/pnas.0405976101
doi: 10.1073/pnas.0405976101 pubmed: 15520376 pmcid: 528957
Pita L, Erwin PM, Turon X, López-Legentil S (2013) Till Death Do Us Part: Stable Sponge-Bacteria Associations under Thermal and Food Shortage Stresses. PLoS ONE 8:e80307. https://doi.org/10.1371/journal.pone.0080307
doi: 10.1371/journal.pone.0080307 pubmed: 24312210 pmcid: 3842930
Pita L, Rix L, Slaby BM et al (2018) The sponge holobiont in a changing ocean: from microbes to ecosystems. Microbiome 6:46. https://doi.org/10.1186/s40168-018-0428-1
doi: 10.1186/s40168-018-0428-1 pubmed: 29523192 pmcid: 5845141
Posadas N, Baquiran JIP, Nada MAL et al (2022) Microbiome diversity and host immune functions influence survivorship of sponge holobionts under future ocean conditions. ISME J 16:58–67. https://doi.org/10.1038/s41396-021-01050-5
doi: 10.1038/s41396-021-01050-5 pubmed: 34218251
Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219
doi: 10.1093/nar/gks1219 pubmed: 23193283
Radeke HS, Digits CA, Casaubon RL, Snapper ML (1999) Interactions of (−)-ilimaquinone with methylation enzymes: implications for vesicular-mediated secretion. Chem Biol 6:639–647. https://doi.org/10.1016/S1074-5521(99)80115-X
doi: 10.1016/S1074-5521(99)80115-X pubmed: 10467129
Risely A (2020) Applying the core microbiome to understand host–microbe systems. J Anim Ecol 89:1549–1558. https://doi.org/10.1111/1365-2656.13229
doi: 10.1111/1365-2656.13229 pubmed: 32248522
Roberts DE, Davis AR, Cummins SP (2006) Experimental manipulation of shade, silt, nutrients and salinity on the temperate reef sponge Cymbastela concentrica. Mar Ecol Prog Ser 307:143–154. https://doi.org/10.3354/meps307143
doi: 10.3354/meps307143
Ruiz C, Valderrama K, Zea S, Castellanos L (2013) Mariculture and natural production of the antitumoural (+)-discodermolide by the Caribbean marine sponge Discodermia dissoluta. Mar Biotechnol 15:571–583. https://doi.org/10.1007/s10126-013-9510-7
doi: 10.1007/s10126-013-9510-7
Schiefenhövel K, Kunzmann A (2012) Sponge Farming Trials: Survival, Attachment, and Growth of Two Indo-Pacific Sponges, Neopetrosia sp. and Stylissa massa. J Marine Sci 2012:417360. https://doi.org/10.1155/2012/417360
doi: 10.1155/2012/417360
Schmitt S, Hentschel U, Taylor MW (2012) Deep sequencing reveals diversity and community structure of complex microbiota in five Mediterranean sponges. Hydrobiologia 687:341–351. https://doi.org/10.1007/s10750-011-0799-9
doi: 10.1007/s10750-011-0799-9
Schmitt S, Tsai P, Bell J et al (2012) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 6:564–576. https://doi.org/10.1038/ismej.2011.116
doi: 10.1038/ismej.2011.116 pubmed: 21993395
Schuster A, Knapp IS, Pomponi SA et al (2016) Validation of RAD-Seq for sponge phylogenetics. Poster in Gesellschaft für Biologische Systematik (GfBS), Munich. https://doi.org/10.13140/RG.2.1.3868.1362
Sipkema D, Franssen MCR, Osinga R et al (2005) Marine Sponges as Pharmacy. Mar. Biotechnol 7:142–162. https://doi.org/10.1007/s10126-004-0405-5
doi: 10.1007/s10126-004-0405-5
Sipkema D, Osinga R, Schatton W et al (2005) Large-scale production of pharmaceuticals by marine sponges: Sea, cell, or synthesis? Biotechnol Bioeng 90:201–222. https://doi.org/10.1002/bit.20404
doi: 10.1002/bit.20404 pubmed: 15739169
Slaby BM, Franke A, Rix L et al (2019) Marine sponge holobionts in health and disease. In: Li Z (ed) Symbiotic Microbiomes of Coral Reefs Sponges and Corals. Springer, Netherlands, Dordrecht, pp 81–104
doi: 10.1007/978-94-024-1612-1_7
Smith FGW (1941) Sponge disease in British Honduras, and its transmission by water currents. Ecology 22:415–421. https://doi.org/10.2307/1930719
doi: 10.2307/1930719
Steffen K, Indraningrat AAG, Erngren I et al (2022) Oceanographic setting influences the prokaryotic community and metabolome in deep-sea sponges. Sci Rep 12:3356. https://doi.org/10.1038/s41598-022-07292-3
doi: 10.1038/s41598-022-07292-3 pubmed: 35233042 pmcid: 8888554
Strand R, Whalan S, Webster NS et al (2017) The response of a boreal deep-sea sponge holobiont to acute thermal stress. Sci Rep 7:1660. https://doi.org/10.1038/s41598-017-01091-x
doi: 10.1038/s41598-017-01091-x pubmed: 28533520 pmcid: 5440399
Swierts T, Cleary DFR, de Voogd NJ (2018) Prokaryotic communities of Indo-Pacific giant barrel sponges are more strongly influenced by geography than host phylogeny. FEMS Microbiology Ecology 94. https://doi.org/10.1093/femsec/fiy194
Taylor MW, Schupp PJ, Dahllöf I et al (2004) Host specificity in marine sponge-associated bacteria, and potential implications for marine microbial diversity. Environ Microbiol 6:121–130. https://doi.org/10.1046/j.1462-2920.2003.00545.x
doi: 10.1046/j.1462-2920.2003.00545.x pubmed: 14756877
Taylor MW, Hill RT, Piel J et al (2007) Soaking it up: the complex lives of marine sponges and their microbial associates. ISME J 1:187–190. https://doi.org/10.1038/ismej.2007.32
doi: 10.1038/ismej.2007.32 pubmed: 18043629
Ternon E, Perino E, Manconi R et al (2017) How Environmental Factors Affect the Production of Guanidine Alkaloids by the Mediterranean Sponge Crambe crambe. Mar Drugs 15:181. https://doi.org/10.3390/md15060181
doi: 10.3390/md15060181 pubmed: 28621725 pmcid: 5484131
Thomas T, Moitinho-Silva L, Lurgi M et al (2016) Diversity, structure and convergent evolution of the global sponge microbiome. Nat Commun 7:11870. https://doi.org/10.1038/ncomms11870
doi: 10.1038/ncomms11870 pubmed: 27306690 pmcid: 4912640
Thoms C, Horn M, Wagner M et al (2003) Monitoring microbial diversity and natural product profiles of the sponge Aplysina cavernicola following transplantation. Mar Biol 142:685–692. https://doi.org/10.1007/s00227-002-1000-9
doi: 10.1007/s00227-002-1000-9
Thoms C, Schupp PJ, Custódio MR et al (2007) Chemical defense strategies in sponges: a review. Porifera Res: Biodiverse Innov Sustain 28:627–637
Turnbaugh PJ, Ley RE, Hamady M et al (2007) The Human Microbiome Project. Nature 449:804–810. https://doi.org/10.1038/nature06244
doi: 10.1038/nature06244 pubmed: 17943116 pmcid: 3709439
van Treeck P, Eisinger M, Müller J et al (2003) Mariculture trials with Mediterranean sponge species: The exploitation of an old natural resource with sustainable and novel methods. Aquaculture 218:439–455. https://doi.org/10.1016/S0044-8486(03)00010-3
doi: 10.1016/S0044-8486(03)00010-3
Vavrek M (2011) Fossil: Palaeoecological and Palaeogeographical Analysis Tools. Palaeontol Electron 14:16
Voultsiadou E (2007) Sponges: an historical survey of their knowledge in Greek antiquity. J Mar Biol Assoc UK 87:1757–1763. https://doi.org/10.1017/S0025315407057773
doi: 10.1017/S0025315407057773
Webster NS, Cobb RE, Negri AP (2008) Temperature thresholds for bacterial symbiosis with a sponge. ISME J 2:830–842. https://doi.org/10.1038/ismej.2008.42
doi: 10.1038/ismej.2008.42 pubmed: 18480849
Weigel BL, Erwin PM (2017) Effects of reciprocal transplantation on the microbiome and putative nitrogen cycling functions of the intertidal sponge. Hymeniacidon Heliophila Sci Rep 7:43247. https://doi.org/10.1038/srep43247
doi: 10.1038/srep43247 pubmed: 28233813
Wilson MC, Mori T, Rückert C et al (2014) An environmental bacterial taxon with a large and distinct metabolic repertoire. Nature 506:58–62. https://doi.org/10.1038/nature12959
doi: 10.1038/nature12959 pubmed: 24476823
World Meteorological Association (2022) State of the global climate 2021. World Meteorological Organization, Geneva, Switzerland. No. 1290
Wulff J (2001) Assessing and monitoring coral reef sponges: Why and how? Bull Mar Sci 69:831–846
Yang Q, Franco CMM, Lin H-W, Zhang W (2019) Untapped sponge microbiomes: structure specificity at host order and family levels. FEMS Microbiology Ecology 95:fiz136. https://doi.org/10.1093/femsec/fiz136
doi: 10.1093/femsec/fiz136 pubmed: 31494678
Yasuhara-Bell J, Lu Y (2010) Marine compounds and their antiviral activities. Antiviral Res 86:231–240. https://doi.org/10.1016/j.antiviral.2010.03.009
doi: 10.1016/j.antiviral.2010.03.009 pubmed: 20338196 pmcid: 7132374
Zaneveld JR, McMinds R, Vega Thurber R (2017) Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat Microbiol 2:1–8. https://doi.org/10.1038/nmicrobiol.2017.121
doi: 10.1038/nmicrobiol.2017.121

Auteurs

Mathilde Maslin (M)

Univ Polynesie Française, Ifremer, ILM, IRD, EIO UMR 241, Tahiti, French Polynesia.

Benoît Paix (B)

Naturalis Biodiversity Center, PO Box 9517, 2300 RA, Leiden, the Netherlands. benoit.paix@gmail.com.

Niels van der Windt (N)

Naturalis Biodiversity Center, PO Box 9517, 2300 RA, Leiden, the Netherlands.
Institute of Environmental Sciences (CML), Leiden University, PO Box 9518, 2300 RA, Leiden, the Netherlands.

Rohani Ambo-Rappe (R)

Faculty of Marine Science and Fisheries, Department of Marine Science, Hasanuddin University, Makassar, Indonesia.

Cécile Debitus (C)

IRD, Univ Brest, CNRS, Ifremer, LEMAR, 29280, Plouzané, France.

Nabila Gaertner-Mazouni (N)

Univ Polynesie Française, Ifremer, ILM, IRD, EIO UMR 241, Tahiti, French Polynesia.

Raimana Ho (R)

Univ Polynesie Française, Ifremer, ILM, IRD, EIO UMR 241, Tahiti, French Polynesia.

Nicole J de Voogd (NJ)

Naturalis Biodiversity Center, PO Box 9517, 2300 RA, Leiden, the Netherlands. n.j.de.voogd@biology.leidenuniv.nl.
Institute of Biology (IBL), Leiden University, 2333 BE, PO Box 9505, Leiden, the Netherlands. n.j.de.voogd@biology.leidenuniv.nl.

Classifications MeSH