A comparison of free-living and sponge-associated bacterial communities from a remote oceanic island with a focus on calcareous sponges

Cleary, D. F. R.; Oliveira, V.; Gomes, N. C. M.; Bialecki, A.; de Voogd, N. J.

doi:10.1093/femsec/fiad014

Title: A comparison of free-living and sponge-associated bacterial communities from a remote oceanic island with a focus on calcareous sponges

Journal Article · 08 February 2023 · FEMS Microbiology Ecology (Online)

DOI: https://doi.org/10.1093/femsec/fiad014 · OSTI ID:1962126

; Oliveira, V.; Gomes, N. C. M.; Bialecki, A.; de Voogd, N. J.

Abstract Calcareous sponges are an often overlooked element of sponge communities. In contrast to most other sponges, calcareous sponges produce calcium carbonate spicules, as opposed to the siliceous spicules of most sponges. Here, we investigated the bacterial communities of 17 sponge species, including type and paratype specimens of recently described calcareous species, sampled off the remote island of Rodrigues, in the Indian Ocean. The main axis of variation in a PCO analysis of all samples separated noncalcareous sponge species, including Axinyssa aplysinoides, Cinachyrella aff. australiensis, Petrosia seychellensis, Ircinia aff. variabilis, Spongia ceylonensis, Plakinastrella aff. clipptertonensis, Agelas aff. ceylonica, Agelas aff. mauritiana, and Hyrtios erectus from calcareous sponges, the noncalcareous Biemna tubulata, sediment, and seawater. Overall, the bacterial communities of calcareous sponges revealed unique prokaryotic profiles with low abundances of several bacterial phyla, and relatively high abundances of other taxa, for example, the phyla Fibrobacterota, Proteobacteria, and the SAR324 clade, the class Alphaproteobacteria, and orders Cytophagales and Cyanobacteriales, although there was considerable variation among species. Calcareous sponges also had a high dominance of unknown bacterial operational taxonomic units (OTUs). Considering the unique nature of these communities, further studies are needed to better understand the environmental and ecological drivers of calcareous sponge-associated bacterial communities and their relevance as potential sources of novel microbes of biotechnological interest.

View Journal Article

Cite

Export

Save

Sponsoring Organization:: USDOE Office of Electricity (OE); USDOE Office of Nuclear Energy (NE), Nuclear Fuel Cycle and Supply Chain

OSTI ID:: 1962126

Journal Information:: FEMS Microbiology Ecology (Online), Journal Name: FEMS Microbiology Ecology (Online) Journal Issue: 3 Vol. 99; ISSN 1574-6941

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: Netherlands

Language:: English

References (64)

The Order Cytophagales Reichenbach, Hans The Prokaryotes https://doi.org/10.1007/0-387-30747-8_20	book	January 2006
Systema Porifera. A Guide to the Classification of Sponges Hooper, John N. A.; Van Soest, Rob W. M. Systema Porifera https://doi.org/10.1007/978-1-4615-0747-5_1	book	January 2002
The Phylum Gemmatimonadetes Hanada, Satoshi; Sekiguchi, Yuji The Prokaryotes https://doi.org/10.1007/978-3-642-38954-2_164	book	January 2014
Microbial Diversity of Marine Sponges Hentschel, U.; Fieseler, L.; Wehrl, M. Sponges (Porifera) https://doi.org/10.1007/978-3-642-55519-0_3	book	January 2003
The Fibrobacteres: an Important Phylum of Cellulose-Degrading Bacteria Ransom-Jones, Emma; Jones, David L.; McCarthy, Alan J. Microbial Ecology, Vol. 63, Issue 2 https://doi.org/10.1007/s00248-011-9998-1	journal	January 2012
Composition and Predictive Functional Analysis of Bacterial Communities in Seawater, Sediment and Sponges in the Spermonde Archipelago, Indonesia Cleary, Daniel F. R.; de Voogd, Nicole J.; Polónia, Ana R. M. Microbial Ecology, Vol. 70, Issue 4 https://doi.org/10.1007/s00248-015-0632-5	journal	June 2015
Bacterial Communities Inhabiting the Sponge Biemna fortis, Sediment and Water in Marine Lakes and the Open Sea Cleary, Daniel F. R.; Polónia, Ana R. M.; de Voogd, Nicole J. Microbial Ecology, Vol. 76, Issue 3 https://doi.org/10.1007/s00248-018-1156-6	journal	February 2018
Prokaryote Communities Inhabiting Endemic and Newly Discovered Sponges and Octocorals from the Red Sea Cleary, D. F. R.; Polónia, A. R. M.; Reijnen, B. T. Microbial Ecology, Vol. 80, Issue 1 https://doi.org/10.1007/s00248-019-01465-w	journal	January 2020
Marine Sponges as Pharmacy Sipkema, Detmer; Franssen, Maurice C. R.; Osinga, Ronald Marine Biotechnology, Vol. 7, Issue 3 https://doi.org/10.1007/s10126-004-0405-5	journal	March 2005
Compositional analysis of bacterial communities in seawater, sediment, and sponges in the Misool coral reef system, Indonesia Cleary, Daniel Francis Richard; Polónia, Ana Rita Moura; Becking, Leontine E. Marine Biodiversity, Vol. 48, Issue 4 https://doi.org/10.1007/s12526-017-0697-0	journal	April 2017
Electron microscope study of the association between some sponges and bacteria Vacelet, Jean; Donadey, Claude Journal of Experimental Marine Biology and Ecology, Vol. 30, Issue 3 https://doi.org/10.1016/0022-0981(77)90038-7	journal	January 1977
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Cultivation of marine sponges for metabolite production: Applications for biotechnology? Osinga, Ronald; Tramper, Johannes; Wijffels, René H. Trends in Biotechnology, Vol. 16, Issue 3 https://doi.org/10.1016/S0167-7799(97)01164-5	journal	March 1998
Metabolic model of nitrite reduction to nitrous oxide coupled to alternating consumption and storage of glycogen and polyhydroxyalkanoate Wang, Zhiyue; Pane, Vince E.; Criddle, Craig S. Bioresource Technology Reports, Vol. 9 https://doi.org/10.1016/j.biteb.2019.100370	journal	February 2020
The functional roles of marine sponges Bell, James J. Estuarine, Coastal and Shelf Science, Vol. 79, Issue 3 https://doi.org/10.1016/j.ecss.2008.05.002	journal	September 2008
Pharmaceutically active secondary metabolites of marine actinobacteria Manivasagan, Panchanathan; Venkatesan, Jayachandran; Sivakumar, Kannan Microbiological Research, Vol. 169, Issue 4 https://doi.org/10.1016/j.micres.2013.07.014	journal	April 2014
A New Perspective on Microbes Formerly Known as Nitrite-Oxidizing Bacteria Daims, Holger; Lücker, Sebastian; Wagner, Michael Trends in Microbiology, Vol. 24, Issue 9 https://doi.org/10.1016/j.tim.2016.05.004	journal	September 2016
Insights into the evolution of freshwater sponges (Porifera: Demospongiae: Spongillina): Barcoding and phylogenetic data from Lake Tanganyika endemics indicate multiple invasions and unsettle existing taxonomy Erpenbeck, Dirk; Weier, Tina; de Voogd, Nicole J. Molecular Phylogenetics and Evolution, Vol. 61, Issue 1 https://doi.org/10.1016/j.ympev.2011.05.021	journal	October 2011
Occurrence of Paraleucilla magna (Porifera: Calcarea) in the Mediterranean Sea Longo, Caterina; Mastrototaro, Francesco; Corriero, Giuseppe Journal of the Marine Biological Association of the United Kingdom, Vol. 87, Issue 6 https://doi.org/10.1017/S0025315407057748	journal	December 2007
Characterization of Leucetta prolifera, a calcarean cyanosponge from south-western Australia, and its symbionts Fromont, Jane; Huggett, Megan J.; Lengger, Sabine K. Journal of the Marine Biological Association of the United Kingdom, Vol. 96, Issue 2 https://doi.org/10.1017/S0025315415000491	journal	September 2015
Diversity, structure and convergent evolution of the global sponge microbiome Thomas, Torsten; Moitinho-Silva, Lucas; Lurgi, Miguel Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11870	journal	June 2016
DADA2: High-resolution sample inference from Illumina amplicon data Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3869	journal	May 2016
Genomic insights into the marine sponge microbiome Hentschel, Ute; Piel, Jörn; Degnan, Sandie M. Nature Reviews Microbiology, Vol. 10, Issue 9 https://doi.org/10.1038/nrmicro2839	journal	July 2012
Marine Dadabacteria exhibit genome streamlining and phototrophy-driven niche partitioning Graham, Elaina D.; Tully, Benjamin J. The ISME Journal, Vol. 15, Issue 4 https://doi.org/10.1038/s41396-020-00834-5	journal	November 2020
The sponge microbiome within the greater coral reef microbial metacommunity Cleary, Daniel F. R.; Swierts, Thomas; Coelho, Francisco J. R. C. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-09537-8	journal	April 2019
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 Bolyen, Evan; Rideout, Jai Ram; Dillon, Matthew R. Nature Biotechnology, Vol. 37, Issue 8 https://doi.org/10.1038/s41587-019-0209-9	journal	July 2019
Expressed protein profile of a Tectomicrobium and other microbial symbionts in the marine sponge Aplysina aerophoba as evidenced by metaproteomics Chaib De Mares, Maryam; Jiménez, Diego Javier; Palladino, Giorgia Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-30134-0	journal	August 2018
Genomic blueprints of sponge-prokaryote symbiosis are shared by low abundant and cultivatable Alphaproteobacteria Karimi, Elham; Keller-Costa, Tina; Slaby, Beate M. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-38737-x	journal	February 2019
Deciphering the unique cellulose degradation mechanism of the ruminal bacterium Fibrobacter succinogenes S85 Raut, Mahendra P.; Couto, Narciso; Karunakaran, Esther Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-52675-8	journal	November 2019
Characterizing the microbiomes of Antarctic sponges: a functional metagenomic approach Moreno-Pino, Mario; Cristi, Antonia; Gillooly, James F. Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-57464-2	journal	January 2020
Metabolites from symbiotic bacteria Piel, Jörn Nat. Prod. Rep., Vol. 26, Issue 3 https://doi.org/10.1039/B703499G	journal	January 2009
Assessing calcareous sponges and their associated bacteria for the discovery of new bioactive natural products Roué, Mélanie; Quévrain, Elodie; Domart-Coulon, Isabelle Natural Product Reports, Vol. 29, Issue 7 https://doi.org/10.1039/c2np20040f	journal	January 2012
Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts Fan, L.; Reynolds, D.; Liu, M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 27 https://doi.org/10.1073/pnas.1203287109	journal	June 2012
XXXVI.—Contributions to our knowledge of the Spongida Carter, H. J. Annals and Magazine of Natural History, Vol. 12, Issue 71 https://doi.org/10.1080/00222938309459636	journal	November 1883
Prokaryotic communities of Indo-Pacific giant barrel sponges are more strongly influenced by geography than host phylogeny Swierts, T.; Cleary, D. F. R.; de Voogd, N. J. FEMS Microbiology Ecology, Vol. 94, Issue 12 https://doi.org/10.1093/femsec/fiy194	journal	October 2018
Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies Klindworth, Anna; Pruesse, Elmar; Schweer, Timmy Nucleic Acids Research, Vol. 41, Issue 1 https://doi.org/10.1093/nar/gks808	journal	August 2012
Recharacterization and Emended Description of the Genus Mycoplana and Description of Two New Species, Mycoplana ramosa and Mycoplana segnis Urakami, T.; Oyanagi, H.; Araki, H. International Journal of Systematic Bacteriology, Vol. 40, Issue 4 https://doi.org/10.1099/00207713-40-4-434	journal	October 1990
Refining the taxonomic structure of the phylum Acidobacteria Dedysh, Svetlana N.; Yilmaz, Pelin International Journal of Systematic and Evolutionary Microbiology, Vol. 68, Issue 12 https://doi.org/10.1099/ijsem.0.003062	journal	December 2018
Habitat- and host-related variation in sponge bacterial symbiont communities in Indonesian waters Cleary, Daniel F. R.; Becking, Leontine E.; de Voogd, Nicole J. FEMS Microbiology Ecology, Vol. 85, Issue 3 https://doi.org/10.1111/1574-6941.12135	journal	May 2013
Diversity and antimicrobial activities of microbes from two Irish marine sponges, Suberites carnosus and Leucosolenia sp. Flemer, B.; Kennedy, J.; Margassery, L. M. Journal of Applied Microbiology, Vol. 112, Issue 2 https://doi.org/10.1111/j.1365-2672.2011.05211.x	journal	December 2011
Partial Carbon and Energy Budgets of the Bacteriosponge Verohgia fistularis (Porifera: Demospongiae) in Barbados Reiswig, Henry M. Marine Ecology, Vol. 2, Issue 4 https://doi.org/10.1111/j.1439-0485.1981.tb00271.x	journal	December 1981
Evidence for spicule homology in calcareous and siliceous sponges: biminerallic spicules inLenicasp. from the Early Cambrian of South China Botting, Joseph P.; Muir, Lucy A.; Xiao, Shuhai Lethaia, Vol. 45, Issue 4 https://doi.org/10.1111/j.1502-3931.2012.00308.x	journal	April 2012
Marine sponges as microbial fermenters: Marine sponges as microbial fermenters Hentschel, Ute; Usher, Kayley M.; Taylor, Michael W. FEMS Microbiology Ecology, Vol. 55, Issue 2 https://doi.org/10.1111/j.1574-6941.2005.00046.x	journal	February 2006
Assessing the bacterial communities of sponges inhabiting the remote western Indian Ocean island of Mayotte de Voogd, Nicole J.; Gauvin-Bialecki, Anne; Polónia, Ana R. M. Marine Ecology, Vol. 39, Issue 6 https://doi.org/10.1111/maec.12517	journal	December 2018
Composition and diversity of prokaryotic communities sampled from sponges and soft corals in Maldivian waters Cleary, Daniel Francis Richard; Polónia, Ana Rita Moura; de Voogd, Nicole Joy Marine Ecology, Vol. 42, Issue 2 https://doi.org/10.1111/maec.12638	journal	March 2021
Microbial Diversity and Putative Diazotrophy in High- and Low-Microbial-Abundance Mediterranean Sponges Ribes, Marta; Dziallas, Claudia; Coma, Rafel Applied and Environmental Microbiology, Vol. 81, Issue 17 https://doi.org/10.1128/AEM.01320-15	journal	September 2015
Complete Genome Sequence of Nitrosospira multiformis, an Ammonia-Oxidizing Bacterium from the Soil Environment Norton, J. M.; Klotz, M. G.; Stein, L. Y. Applied and Environmental Microbiology, Vol. 74, Issue 11 https://doi.org/10.1128/AEM.02722-07	journal	April 2008
Molecular Evidence for a Uniform Microbial Community in Sponges from Different Oceans Hentschel, U.; Hopke, J.; Horn, M. Applied and Environmental Microbiology, Vol. 68, Issue 9 https://doi.org/10.1128/AEM.68.9.4431-4440.2002	journal	September 2002
Fiber-Degrading Systems of Different Strains of the Genus Fibrobacter Bera-Maillet, C.; Ribot, Y.; Forano, E. Applied and Environmental Microbiology, Vol. 70, Issue 4 https://doi.org/10.1128/AEM.70.4.2172-2179.2004	journal	April 2004
A Robust Species Tree for the Alphaproteobacteria Williams, K. P.; Sobral, B. W.; Dickerman, A. W. Journal of Bacteriology, Vol. 189, Issue 13 https://doi.org/10.1128/JB.00269-07	journal	May 2007
Sponge-Associated Microorganisms: Evolution, Ecology, and Biotechnological Potential Taylor, M. W.; Radax, R.; Steger, D. Microbiology and Molecular Biology Reviews, Vol. 71, Issue 2 https://doi.org/10.1128/MMBR.00040-06	journal	June 2007
Calcareous sponges of Indonesia Soest, Rob W. M. Van Zootaxa, Vol. 3951, Issue 1 https://doi.org/10.11646/zootaxa.3951.1.1	journal	April 2015
Calcareous sponges of the Western Indian Ocean and Red Sea Van Soest, Rob W. M.; De Voogd, Nicole J. Zootaxa, Vol. 4426, Issue 1 https://doi.org/10.11646/zootaxa.4426.1.1	journal	June 2018
Molecular Phylogenetic Evaluation of Classification and Scenarios of Character Evolution in Calcareous Sponges (Porifera, Class Calcarea) Voigt, Oliver; Wülfing, Eilika; Wörheide, Gert PLoS ONE, Vol. 7, Issue 3 https://doi.org/10.1371/journal.pone.0033417	journal	March 2012
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data McMurdie, Paul J.; Holmes, Susan PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061217	journal	April 2013
Feature Selection with the Boruta Package Kursa, Miron B.; Rudnicki, Witold R. Journal of Statistical Software, Vol. 36, Issue 11 https://doi.org/10.18637/jss.v036.i11	journal	January 2010
Diet Composition of Two Temperate Calcareous Sponges: Leucosolenia echinata and Leucetta sp. from the Wellington South Coast, New Zealand Perea-Blázquez, Alejandra The Open Marine Biology Journal, Vol. 4, Issue 1 https://doi.org/10.2174/1874450801004010065	journal	October 2010
Boruta – A System for Feature Selection Kursa, Miron B.; Jankowski, Aleksander; Rudnicki, Witold R. Fundamenta Informaticae, Vol. 101, Issue 4 https://doi.org/10.3233/FI-2010-288	journal	January 2010
Carbonic Anhydrases: An Ancient Tool in Calcareous Sponge Biomineralization Voigt, Oliver; Fradusco, Benedetta; Gut, Carolin Frontiers in Genetics, Vol. 12 https://doi.org/10.3389/fgene.2021.624533	journal	April 2021
Predicting the HMA-LMA Status in Marine Sponges by Machine Learning Moitinho-Silva, Lucas; Steinert, Georg; Nielsen, Shaun Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00752	journal	May 2017
Cultivation-Independent Analysis of the Bacterial Community Associated With the Calcareous Sponge Clathrina clathrus and Isolation of Poriferisphaera corsica Gen. Nov., Sp. Nov., Belonging to the Barely Studied Class Phycisphaerae in the Phylum Planctomycetes Kallscheuer, Nicolai; Wiegand, Sandra; Kohn, Timo Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.602250	journal	December 2020
Variability in Host Specificity and Functional Potential of Antarctic Sponge-Associated Bacterial Communities Cristi, Antonia; Parada-Pozo, Génesis; Morales-Vicencio, Felipe Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.771589	journal	January 2022
Phylogeny and Metabolic Potential of the Candidate Phylum SAR324 Malfertheiner, Lukas; Martínez-Pérez, Clara; Zhao, Zihao Biology, Vol. 11, Issue 4 https://doi.org/10.3390/biology11040599	journal	April 2022
A sea surface temperature reconstruction for the southern Indian Ocean trade wind belt from corals in Rodrigues Island (19° S, 63° E) Zinke, Jens; Reuning, Lars; Pfeiffer, Miriam Biogeosciences, Vol. 13, Issue 20 https://doi.org/10.5194/bg-13-5827-2016	journal	January 2016

Similar Records

Impacts of humic substances, elevated temperature, and UVB radiation on bacterial communities of the marine sponge Chondrilla sp

Journal Article · 2024 · FEMS Microbiology Ecology (Online) · OSTI ID:2317706

Stuij, Tamara M.; Cleary, Daniel F. R.; Rocha, Rui J. M.; +5 more

Vertical stratification of subsurface microbial community composition across geological formations at the Hanford Site

Journal Article · 2011 · Environmental Microbiology, 14(2):414-425 · OSTI ID:1034978

Lin, Xueju; Kennedy, David W; Fredrickson, Jim K; +2 more

Taxonomic and Functional Microbial Signatures of the Endemic Marine Sponge Arenosclera brasiliensis

Journal Article · 2012 · PLoS ONE · OSTI ID:1627531

Trindade-Silva, Amaro E.; Rua, Cintia; Silva, Genivaldo G. Z.; +8 more

Title: A comparison of free-living and sponge-associated bacterial communities from a remote oceanic island with a focus on calcareous sponges

Citation Formats

References (64)

Similar Records

Related Subjects