Wikipedia

Sponge microbiomes

Sponge microbiomes are diverse communities of microorganisms in symbiotic association with marine sponges as their hosts.[2] These microorganisms include bacteria, archaea, fungi, viruses, among others.[3] The sponges have the ability to filter seawater and recycle nutrients while providing a safe habitat to many microorganisms, which provide the sponge host with fixed nitrogen and carbon, and stimulates the immune system.[3][4] Together, a sponge and its microbiome form a holobiont, with a single sponge often containing more than 40 bacterial phyla, making sponge microbial environments a diverse and dense community.[2][5][6] Furthermore, individual holobionts work hand in hand with other near holobionts becoming a nested ecosystem, affecting the environment at multiple scales.[3]

Sponges and their microbiomes are considered a holobiont.[1]

Composition

edit

Microbiome species diversity

edit
 
A heatmap of the taxonnomic profiles of microbial communities in different sponge species.[7]

Microbial composition in sponges can differ based on the amount of light the microbes have access to. The outer layer of sponge, which is exposed to light, is usually inhabited by photosynthetically active microorganisms, such as Cyanobacteria, whereas the inner portion of the sponge is dominated by heterotrophic microbes.[8] Shallow-water sponges in particular form complex host-microbe relationships within the marine ecosystem, with over 40 bacterial phyla identifiable on a sponge individual.[2] Deep-sea sponge microbes are less diverse overall, but have more varied compositions between individual sponge organisms.[5] Although there are common microorganism species shared by both shallow-water sponges and deep-sea sponges, many microbial species differ between the two sponges. For example, Chloroflexota was found in higher abundance in deep-sea sponges compared to shallow ones.

Sponges can be classified as High Microbial Abundance (HMA) sponges and Low Microbial Abundance (LMA) sponges based on the density of microorganisms they host.[9] HMA sponges are specifically characterized by their capacity to support a 1010 cells per gram of sponge tissue, whereas LMA sponges are defined by a much lower density of 106 cells per gram of sponge tissue.[10] In HMA sponges, up to one third of the overall sponge biomass can be microbial biomass.[11] Chloroflexota, Gammaproteobacteria, and Alphaproteobacteria are phyla and subphyla that have been reported to characterize HMA species.[12] The HMA sponge communities were found to be complex, and are dominated by Proteobacteria, Cyanobacteria, Bacteroidetes, Acidobacteria, and Planctomycetes in the samples from Montgri Coast (northwest Mediterranean Sea).[13] In contrast, LMA sponge communities have restricted the number of microbe species, including Proteobacteria and Cyanobacteria.[9][11]

Symbiont acquisition

edit

Sponge-specific symbionts are hypothesized to have begun their association with sponges as long as 600 million years ago, but there are several hypotheses as to how the microbes colonized and continued to inhabit sponges.[14] The most evidenced hypothesis of sponge-specific symbionts says that sponges were colonized prior to sponge speciation, during the Precambrian period.[15] This colonization is thought to have been maintained throughout the years by vertical transmission, which resulted in microbial species diverging alongside sponge species.[2] Support for this hypothesis comes from the presence of fatty acids within sponges that are not present within the surrounding environment. These fatty acids are of microbial origin and appear within many different sponge species that share neither location nor ancestry, indicating that the microbial producers of these fatty acids colonized sponges before the sponge species differentiated.[16] However, this hypothesis is still only a hypothesis, and it requires more evidence before it (or other hypotheses of microbe acquisition) can be confirmed.

Ecological functions

edit

Carbon metabolism

edit

Marine sponges are commonly heterotrophic, getting their carbon from dissolved organic material or consumption of microorganisms.[17] However, transfer of organic carbon from the microbiome to the sponge host has been demonstrated in several sponge species.[17] This is most often observed in tropical sponges that carry dense communities of photosynthetic cyanobacteria, which use sunlight and oxygen to produce organic carbon.[18] Some of that organic carbon is then provided to the sponge, largely in the form of glycerol.[18] Sponges that live in high-light, low-nutrient locations such as tropical reefs rely heavily on organic carbon produced by their symbiotic cyanobacteria, and in some cases have been observed to gain more than 50% of their required energy from this carbon transfer.[18][19] Alternately, sponges living in areas with less available light and higher nutrients (such as areas with higher water turbidity) demonstrate less association with cyanobacteria and less reliance on photosynthesis-derived organic carbon.[20]

A more unusual form of carbon exchange utilizing methane has been observed in carnivorous deep-sea sponges (family Cladorhizidae) living near hydrothermal vents.[21] The level of methanol dehydrogenase present within the sponge tissues indicates that these sponges are host to methanotrophic bacteria, which thrive off of methane gas from nearby hydrothermal vents.[22] Instead of extracellular nutrient transfer (such as with photosynthetic cyanobacteria), most sponge cells are able to phagocytose old or dying bacterial cells, which are then used by the sponge as a source of organic carbon.[22] Cladorhiza species are thought to benefit quite significantly from this symbiosis, as large sponge size and high sponge abundance is correlated with the methane flow of the most active hydrothermal vents, and Cladorhiza species are much less abundant away from the vents.[21]

Nitrogen metabolism

edit

Symbiotic microbes may assist sponges in the acquisition of organic nitrogen in two ways: nitrogen fixation and ammonia oxidation.[17]

Symbiosis with nitrogen-fixing bacteria has been identified in several families of marine sponges through measurement of nitrogenase activity and is particularly beneficial for sponges in low-nitrogen waters, where fixed nitrogen is in very high demand.[17][23] The symbiotic bacteria pull molecular nitrogen from the atmosphere and convert it into ammonia, nitrate, and other organic nitrogen-containing compounds that can then be utilized by the sponges.[17]

 
Methylomirabilis oxyfera

Many sponge species are inhabited by ammonia-oxidizing bacteria or archaea, making ammonia oxidation one of the best-studied symbiotic functions of the sponge microbiome.[18] Symbiotic microbes use ammonium released by the sponges as a byproduct of digestion to fuel ammonia and nitrate oxidation, thus providing more fixed nitrogen for the sponges to use.[24] Sponges’ mechanism of pumping water through their tissues can result in deoxygenated zones, which could allow for microbial denitrification and anaerobic ammonia oxidation to occur.[25] This is supported by the greater presence of genes related to denitrification and ammonia oxidation in sponge microbial communities than in surrounding free-living microbes.[18] However, these communities do not have as many genes for nitric oxide reduction, which may lead to harmful buildup of nitric oxide in sponge tissues.[18] At least one bacterial species (Candidatus Methylomirabilis oxyfera) has been identified in the sponge microbiome as being able to convert nitric oxide directly to oxygen and nitrogen gas, which could alleviate the buildup of nitric oxide and assist with oxygenating inner sponge tissues.[26]

Sulfur metabolism

edit

Unlike carbon and nitrogen metabolism, wherein organic carbon and nitrogen are transferred between sponges and resident microbes, sulfur metabolism within the sponge microbiome only involves the microbiota.[14] The sponge acts as the environment in which sulfur-reducing and sulfur-oxidizing microbes carry out a sulfur cycle.[27] This cycling likely takes place within the anaerobic zones of the sponge, as sulfur reduction is an anaerobic process.[14] Accumulation of hydrogen sulfide – which is produced as a byproduct by sulfur-reducing bacteria and is toxic to sponges – is likely prevented by the presence of sulfur-oxidizing bacteria within the sponge microbiota.[14] Current research suggests that sulfur-oxidizing bacteria may also allow sponges to root in sulfur-rich sediments that would otherwise be uninhabitable.[14]

Synthesis of B Vitamins

edit

B vitamins are an important resource for sponge cell metabolism. Sponges cannot synthesize their own B vitamins and so have no way to acquire these vitamins except through filter-feeding. Therefore, association with a B vitamin synthesizing microbe is favorable for the sponge host and may increase the stability of that microbe's presence in the sponge's microbiome.[28][29][30][4] Through the analysis of transporters from symbionts and microbial phyla, six B vitamins have been detected to have come from sponge microbiomes: thiamine (vitamin B1), riboflavin (vitamin B2), pyridoxine (vitamin B6), biotin (vitamin B7), and cobalamin (B12).[4]

References

edit
  1. ^ Pita, L.; Rix, L.; Slaby, B. M.; Franke, A.; Hentschel, U. (2018-03-09). "The sponge holobiont in a changing ocean: from microbes to ecosystems". Microbiome. 6 (1): 46. doi:10.1186/s40168-018-0428-1. ISSN 2049-2618. PMC 5845141. PMID 29523192.
  2. ^ a b c d Thomas, Torsten; Moitinho-Silva, Lucas; Lurgi, Miguel; Björk, Johannes R.; Easson, Cole; Astudillo-García, Carmen; Olson, Julie B.; Erwin, Patrick M.; López-Legentil, Susanna; Luter, Heidi; Chaves-Fonnegra, Andia; Costa, Rodrigo; Schupp, Peter J.; Steindler, Laura; Erpenbeck, Dirk (2016-06-16). "Diversity, structure and convergent evolution of the global sponge microbiome". Nature Communications. 7 (1): 11870. Bibcode:2016NatCo...711870T. doi:10.1038/ncomms11870. ISSN 2041-1723. PMC 4912640. PMID 27306690.
  3. ^ a b c Pita, L.; Rix, L.; Slaby, B. M.; Franke, A.; Hentschel, U. (2018-03-09). "The sponge holobiont in a changing ocean: from microbes to ecosystems". Microbiome. 6 (1): 46. doi:10.1186/s40168-018-0428-1. ISSN 2049-2618. PMC 5845141. PMID 29523192.
  4. ^ a b c Engelberts, J. Pamela; Robbins, Steven J.; de Goeij, Jasper M.; Aranda, Manuel; Bell, Sara C.; Webster, Nicole S. (May 2020). "Characterization of a sponge microbiome using an integrative genome-centric approach". The ISME Journal. 14 (5): 1100–1110. Bibcode:2020ISMEJ..14.1100E. doi:10.1038/s41396-020-0591-9. ISSN 1751-7362. PMC 7174397. PMID 31992859.
  5. ^ a b Busch, Kathrin; Slaby, Beate M.; Bach, Wolfgang; Boetius, Antje; Clefsen, Ina; Colaço, Ana; Creemers, Marie; Cristobo, Javier; Federwisch, Luisa; Franke, Andre; Gavriilidou, Asimenia; Hethke, Andrea; Kenchington, Ellen; Mienis, Furu; Mills, Sadie (2022-09-02). "Biodiversity, environmental drivers, and sustainability of the global deep-sea sponge microbiome". Nature Communications. 13 (1): 5160. Bibcode:2022NatCo..13.5160B. doi:10.1038/s41467-022-32684-4. ISSN 2041-1723. PMC 9440067. PMID 36056000.
  6. ^ Hentschel, Ute; Piel, Jörn; Degnan, Sandie M.; Taylor, Michael W. (September 2019). "Genomic insights into the marine sponge microbiome". Nature Reviews Microbiology. 10 (9): 641–654. doi:10.1038/nrmicro2839. ISSN 1740-1534. PMID 22842661.
  7. ^ Thomas, Torsten; Moitinho-Silva, Lucas; Lurgi, Miguel; Björk, Johannes R.; Easson, Cole; Astudillo-García, Carmen; Olson, Julie B.; Erwin, Patrick M.; López-Legentil, Susanna; Luter, Heidi; Chaves-Fonnegra, Andia; Costa, Rodrigo; Schupp, Peter J.; Steindler, Laura; Erpenbeck, Dirk (2016-06-16). "Diversity, structure and convergent evolution of the global sponge microbiome". Nature Communications. 7 (1): 11870. Bibcode:2016NatCo...711870T. doi:10.1038/ncomms11870. ISSN 2041-1723. PMC 4912640. PMID 27306690.
  8. ^ Hentschel, U.; Fieseler, L.; Wehrl, M.; Gernert, C.; Steinert, M.; Hacker, J.; Horn, M. (2003), Müller, Werner E. G. (ed.), "Microbial Diversity of Marine Sponges", Sponges (Porifera), vol. 37, Berlin, Heidelberg: Springer, pp. 59–88, doi:10.1007/978-3-642-55519-0_3, ISBN 978-3-642-55519-0, PMID 15825640, retrieved 2024-04-09
  9. ^ a b Hentschel, Ute; Usher, Kayley M.; Taylor, Michael W. (February 2006). "Marine sponges as microbial fermenters". FEMS Microbiology Ecology. 55 (2): 167–177. Bibcode:2006FEMME..55..167H. doi:10.1111/j.1574-6941.2005.00046.x. ISSN 0168-6496. PMID 16420625.
  10. ^ Lesser, Michael P. (December 2023). "Size Effects on Pumping Rates in High Microbial versus Low Microbial Abundance Marine Sponges". Oceans. 4 (4): 394–408. doi:10.3390/oceans4040027. ISSN 2673-1924.
  11. ^ a b Moitinho-Silva, Lucas; Steinert, Georg; Nielsen, Shaun; Hardoim, Cristiane C. P.; Wu, Yu-Chen; McCormack, Grace P.; López-Legentil, Susanna; Marchant, Roman; Webster, Nicole; Thomas, Torsten; Hentschel, Ute (2017). "Predicting the HMA-LMA Status in Marine Sponges by Machine Learning". Frontiers in Microbiology. 8: 752. doi:10.3389/fmicb.2017.00752. ISSN 1664-302X. PMC 5421222. PMID 28533766.
  12. ^ Moitinho-Silva, Lucas; Bayer, Kristina; Cannistraci, Carlo V.; Giles, Emily C.; Ryu, Taewoo; Seridi, Loqmane; Ravasi, Timothy; Hentschel, Ute (March 2014). "Specificity and transcriptional activity of microbiota associated with low and high microbial abundance sponges from the Red Sea". Molecular Ecology. 23 (6): 1348–1363. Bibcode:2014MolEc..23.1348M. doi:10.1111/mec.12365. ISSN 0962-1083. PMID 23957633.
  13. ^ Ribes, Marta; Dziallas, Claudia; Coma, Rafel; Riemann, Lasse (September 2015). Spormann, A. M. (ed.). "Microbial Diversity and Putative Diazotrophy in High- and Low-Microbial-Abundance Mediterranean Sponges". Applied and Environmental Microbiology. 81 (17): 5683–5693. Bibcode:2015ApEnM..81.5683R. doi:10.1128/AEM.01320-15. ISSN 0099-2240. PMC 4551227. PMID 26070678.
  14. ^ a b c d e Thacker, Robert W.; Díaz, Maria Cristina; Kerner, Adeline; Vignes-Lebbe, Régine; Segerdell, Erik; Haendel, Melissa A.; Mungall, Christopher J. (2014-09-08). "The Porifera Ontology (PORO): enhancing sponge systematics with an anatomy ontology". Journal of Biomedical Semantics. 5 (1): 39. doi:10.1186/2041-1480-5-39. ISSN 2041-1480. PMC 4177528. PMID 25276334.
  15. ^ Wilkinson, C. R. (1984-02-22). "Immunological evidence for the Precambrian origin of bacterial symbioses in marine sponges". Proceedings of the Royal Society of London. Series B. Biological Sciences. 220 (1221): 509–518. Bibcode:1984RSPSB.220..509W. doi:10.1098/rspb.1984.0017. ISSN 0080-4649.
  16. ^ Thiel, Volker; Jenisch, Angela; Wörheide, Gert; Löwenberg, Antje; Reitner, Joachim; Michaelis, Walter (1999-01-01). "Mid-chain branched alkanoic acids from "living fossil" demosponges: a link to ancient sedimentary lipids?". Organic Geochemistry. 30 (1): 1–14. Bibcode:1999OrGeo..30....1T. doi:10.1016/S0146-6380(98)00200-9. hdl:11858/00-1735-0000-0001-3403-F. ISSN 0146-6380.
  17. ^ a b c d e Taylor, Michael W.; Radax, Regina; Steger, Doris; Wagner, Michael (June 2007). "Sponge-associated Microorganisms: Evolution, Ecology, and Biotechnological Potential". Microbiology and Molecular Biology Reviews. 71 (2): 295–347. doi:10.1128/MMBR.00040-06. ISSN 1092-2172. PMC 1899876. PMID 17554047.
  18. ^ a b c d e f Webster, Nicole S.; Thomas, Torsten (2016-05-04). Dubilier, Nicole; Collier, R. John (eds.). "The Sponge Hologenome". mBio. 7 (2): e00135-16. doi:10.1128/mBio.00135-16. ISSN 2161-2129. PMC 4850255. PMID 27103626.
  19. ^ Wilkinson, C. R. (1983-01-28). "Net primary productivity in coral reef sponges". Science. 219 (4583): 410–412. Bibcode:1983Sci...219..410W. doi:10.1126/science.219.4583.410. ISSN 0036-8075. PMID 17815320.
  20. ^ Wilkinson, C. R. (1987-06-26). "Interocean differences in size and nutrition of coral reef sponge populations". Science. 236 (4809): 1654–1657. Bibcode:1987Sci...236.1654W. doi:10.1126/science.236.4809.1654. ISSN 0036-8075. PMID 17754318.
  21. ^ a b Vacelet, J.; Boury-Esnault, N. (2002). "A new species of carnivorous deep-sea sponge (Demospongiae: Cladorhizidae) associated with methanotrophic bacteria". Cahiers de Biologie Marine. S2CID 89518839.
  22. ^ a b Vacelet, J.; FialaMedioni, A.; Fisher, C. R.; BouryEsnault, N. (December 1996). "Symbiosis between methane-oxidizing bacteria and a deep-sea carnivorous cladorhizid sponge". Marine Ecology Progress Series. 145 (1–3): 77–85. Bibcode:1996MEPS..145...77V. doi:10.3354/meps145077. ISSN 0171-8630.
  23. ^ Wilkinson, C. R.; Fay, Peter (June 1979). "Nitrogen fixation in coral reef sponges with symbiotic cyanobacteria". Nature. 279 (5713): 527–529. Bibcode:1979Natur.279..527W. doi:10.1038/279527a0. ISSN 1476-4687.
  24. ^ Hoffmann, Friederike; Radax, Regina; Woebken, Dagmar; Holtappels, Moritz; Lavik, Gaute; Rapp, Hans Tore; Schläppy, Marie-Lise; Schleper, Christa; Kuypers, Marcel M. M. (September 2009). "Complex nitrogen cycling in the sponge Geodia barretti". Environmental Microbiology. 11 (9): 2228–2243. Bibcode:2009EnvMi..11.2228H. doi:10.1111/j.1462-2920.2009.01944.x. ISSN 1462-2912. PMID 19453700.
  25. ^ Hoffmann, Friederike; Larsen, Ole; Thiel, Volker; Rapp, Hans Tore; Pape, Thomas; Michaelis, Walter; Reitner, Joachim (January 2005). "An Anaerobic World in Sponges". Geomicrobiology Journal. 22 (1–2): 1–10. Bibcode:2005GmbJ...22....1H. doi:10.1080/01490450590922505. ISSN 0149-0451.
  26. ^ Ettwig, Katharina F.; Butler, Margaret K.; Le Paslier, Denis; Pelletier, Eric; Mangenot, Sophie; Kuypers, Marcel M. M.; Schreiber, Frank; Dutilh, Bas E.; Zedelius, Johannes; de Beer, Dirk; Gloerich, Jolein; Wessels, Hans J. C. T.; van Alen, Theo; Luesken, Francisca; Wu, Ming L. (March 2010). "Nitrite-driven anaerobic methane oxidation by oxygenic bacteria". Nature. 464 (7288): 543–548. Bibcode:2010Natur.464..543E. doi:10.1038/nature08883. hdl:2066/84284. ISSN 1476-4687. PMID 20336137.
  27. ^ Imhoff, J. F.; Trüper, H. G. (March 1976). "Marine sponges as habitats of anaerobic phototrophic bacteria". Microbial Ecology. 3 (1): 1–9. Bibcode:1976MicEc...3....1I. doi:10.1007/BF02011449. ISSN 0095-3628. PMID 24233392.
  28. ^ Liu, Michael; Fan, Lu; Zhong, Ling; Kjelleberg, Staffan; Thomas, Torsten (2012-02-02). "Metaproteogenomic analysis of a community of sponge symbionts". The ISME Journal. 6 (8): 1515–1525. Bibcode:2012ISMEJ...6.1515L. doi:10.1038/ismej.2012.1. ISSN 1751-7362. PMC 3400405. PMID 22297557.
  29. ^ Thomas, Torsten; Rusch, Doug; Demaere, Matt Z.; Yung, Pui Yi; Lewis, Matt; Halpern, Aaron; Heidelberg, Karla B.; Egan, Suhelen; Steinberg, Peter D.; Kjelleberg, Staffan (2010). "Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis". The ISME Journal. 4 (12): 1557–1567. Bibcode:2010ISMEJ...4.1557T. doi:10.1038/ismej.2010.74. PMID 20520651. Retrieved 2024-04-09.
  30. ^ Fan, Lu; Reynolds, David; Liu, Michael; Stark, Manuel; Kjelleberg, Staffan; Webster, Nicole S.; Thomas, Torsten (2012-07-03). "Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts". Proceedings of the National Academy of Sciences. 109 (27): E1878-87. doi:10.1073/pnas.1203287109. ISSN 0027-8424. PMC 3390844. PMID 22699508.
Retrieved from "https://en.wikipedia.org/w/index.php?title=Sponge_microbiomes&oldid=1226150766"