Sponge microbiomes: Difference between revisions
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=== Overview === |
=== Overview === |
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[[Sponge|Sponges]] (Phylum [[Sponge|Porifera]]) are [[Multicellular organism|multicellular]] [[Heterotroph|heterotrophic]] marine organisms without true organs or a [[nervous system]].<ref name=":7" /> They are early-diverging [[Animal|metazoans]] that are known to form symbiotic relationships with complex communities of [[Microorganism|microorganisms]], and are a key part of most [[Benthic zone|benthic]] marine ecosystems where they can metabolize fundamental resources such as [[carbon]], [[nitrogen]], and [[sulfur]].<ref name=":7">{{Cite journal | |
[[Sponge|Sponges]] (Phylum [[Sponge|Porifera]]) are [[Multicellular organism|multicellular]] [[Heterotroph|heterotrophic]] marine organisms without true organs or a [[nervous system]].<ref name=":7" /> They are early-diverging [[Animal|metazoans]] that are known to form symbiotic relationships with complex communities of [[Microorganism|microorganisms]], and are a key part of most [[Benthic zone|benthic]] marine ecosystems where they can metabolize fundamental resources such as [[carbon]], [[nitrogen]], and [[sulfur]].<ref name=":7">{{Cite journal |last1=Thacker |first1=Robert W. |last2=Díaz |first2=Maria Cristina |last3=Kerner |first3=Adeline |last4=Vignes-Lebbe |first4=Régine |last5=Segerdell |first5=Erik |last6=Haendel |first6=Melissa A. |last7=Mungall |first7=Christopher J. |date=2014-09-08 |title=The Porifera Ontology (PORO): enhancing sponge systematics with an anatomy ontology |journal=Journal of Biomedical Semantics |volume=5 |issue=1 |pages=39 |doi=10.1186/2041-1480-5-39 |doi-access=free |issn=2041-1480 |pmc=4177528 |pmid=25276334}}</ref> |
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[[File:The sponge holobiont.webp|thumb|217x217px|Sponges and their microbiomes are considered a holobiont.<ref>{{Cite journal | |
[[File:The sponge holobiont.webp|thumb|217x217px|Sponges and their microbiomes are considered a holobiont.<ref>{{Cite journal |last1=Pita |first1=L. |last2=Rix |first2=L. |last3=Slaby |first3=B. M. |last4=Franke |first4=A. |last5=Hentschel |first5=U. |date=2018-03-09 |title=The sponge holobiont in a changing ocean: from microbes to ecosystems |journal=Microbiome |language=en |volume=6 |issue=1 |pages=46 |doi=10.1186/s40168-018-0428-1 |doi-access=free |issn=2049-2618 |pmc=5845141 |pmid=29523192}}</ref> ]] |
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Sponge [[Microbiome|microbiomes]] are diverse communities of microorganisms in symbiotic association with marine sponges as their hosts.<ref name=":4">{{Cite journal | |
Sponge [[Microbiome|microbiomes]] are diverse communities of microorganisms in symbiotic association with marine sponges as their hosts.<ref name=":4">{{Cite journal |last1=Thomas |first1=Torsten |last2=Moitinho-Silva |first2=Lucas |last3=Lurgi |first3=Miguel |last4=Björk |first4=Johannes R. |last5=Easson |first5=Cole |last6=Astudillo-García |first6=Carmen |last7=Olson |first7=Julie B. |last8=Erwin |first8=Patrick M. |last9=López-Legentil |first9=Susanna |last10=Luter |first10=Heidi |last11=Chaves-Fonnegra |first11=Andia |last12=Costa |first12=Rodrigo |last13=Schupp |first13=Peter J. |last14=Steindler |first14=Laura |last15=Erpenbeck |first15=Dirk |date=2016-06-16 |title=Diversity, structure and convergent evolution of the global sponge microbiome |journal=Nature Communications |language=en |volume=7 |issue=1 |pages=11870 |doi=10.1038/ncomms11870 |issn=2041-1723 |pmc=4912640 |pmid=27306690|bibcode=2016NatCo...711870T }}</ref> These microorganisms include [[bacteria]], [[archaea]], [[Fungus|fungi]], [[Virus|viruses]], among others.<ref name=":5">{{Cite journal |last1=Pita |first1=L. |last2=Rix |first2=L. |last3=Slaby |first3=B. M. |last4=Franke |first4=A. |last5=Hentschel |first5=U. |date=2018-03-09 |title=The sponge holobiont in a changing ocean: from microbes to ecosystems |journal=Microbiome |volume=6 |issue=1 |pages=46 |doi=10.1186/s40168-018-0428-1 |doi-access=free |issn=2049-2618 |pmc=5845141 |pmid=29523192}}</ref> 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.<ref name=":5" /><ref>{{Cite journal |last1=Engelberts |first1=J. Pamela |last2=Robbins |first2=Steven J. |last3=de Goeij |first3=Jasper M. |last4=Aranda |first4=Manuel |last5=Bell |first5=Sara C. |last6=Webster |first6=Nicole S. |date=May 2020 |title=Characterization of a sponge microbiome using an integrative genome-centric approach |journal=The ISME Journal |volume=14 |issue=5 |pages=1100–1110 |doi=10.1038/s41396-020-0591-9 |issn=1751-7362 |pmc=7174397 |pmid=31992859|bibcode=2020ISMEJ..14.1100E }}</ref> 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.<ref name=":4" /><ref name=":8">{{Cite journal |last1=Busch |first1=Kathrin |last2=Slaby |first2=Beate M. |last3=Bach |first3=Wolfgang |last4=Boetius |first4=Antje |last5=Clefsen |first5=Ina |last6=Colaço |first6=Ana |last7=Creemers |first7=Marie |last8=Cristobo |first8=Javier |last9=Federwisch |first9=Luisa |last10=Franke |first10=Andre |last11=Gavriilidou |first11=Asimenia |last12=Hethke |first12=Andrea |last13=Kenchington |first13=Ellen |last14=Mienis |first14=Furu |last15=Mills |first15=Sadie |date=2022-09-02 |title=Biodiversity, environmental drivers, and sustainability of the global deep-sea sponge microbiome |journal=Nature Communications |language=en |volume=13 |issue=1 |pages=5160 |doi=10.1038/s41467-022-32684-4 |issn=2041-1723 |pmc=9440067 |pmid=36056000|bibcode=2022NatCo..13.5160B }}</ref><ref>{{Cite journal |last1=Hentschel |first1=Ute |last2=Piel |first2=Jörn |last3=Degnan |first3=Sandie M. |last4=Taylor |first4=Michael W. |date=September 2019 |title=Genomic insights into the marine sponge microbiome |url=https://www.nature.com/articles/nrmicro2839 |journal=Nature Reviews Microbiology |language=en |volume=10 |issue=9 |pages=641–654 |doi=10.1038/nrmicro2839 |pmid=22842661 |issn=1740-1534}}</ref> Furthermore, individual holobionts work hand in hand with other near holobionts becoming a nested ecosystem, affecting the environment at multiple scales.<ref name=":5" /> |
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=== Composition === |
=== Composition === |
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==== Microbiome Species Diversity ==== |
==== Microbiome Species Diversity ==== |
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[[File:Taxonnomic profile of microbial communities.jpg|thumb|366x366px|A heatmap of the taxonnomic profiles of microbial communities in different sponge species.<ref>{{Cite journal | |
[[File:Taxonnomic profile of microbial communities.jpg|thumb|366x366px|A heatmap of the taxonnomic profiles of microbial communities in different sponge species.<ref>{{Cite journal |last1=Thomas |first1=Torsten |last2=Moitinho-Silva |first2=Lucas |last3=Lurgi |first3=Miguel |last4=Björk |first4=Johannes R. |last5=Easson |first5=Cole |last6=Astudillo-García |first6=Carmen |last7=Olson |first7=Julie B. |last8=Erwin |first8=Patrick M. |last9=López-Legentil |first9=Susanna |last10=Luter |first10=Heidi |last11=Chaves-Fonnegra |first11=Andia |last12=Costa |first12=Rodrigo |last13=Schupp |first13=Peter J. |last14=Steindler |first14=Laura |last15=Erpenbeck |first15=Dirk |date=2016-06-16 |title=Diversity, structure and convergent evolution of the global sponge microbiome |journal=Nature Communications |language=en |volume=7 |issue=1 |page=11870 |doi=10.1038/ncomms11870 |issn=2041-1723 |pmc=4912640 |pmid=27306690|bibcode=2016NatCo...711870T }}</ref>]] |
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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 [[Heterotroph|heterotrophic]] microbes.<ref>{{Citation | |
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 [[Heterotroph|heterotrophic]] microbes.<ref>{{Citation |last1=Hentschel |first1=U. |title=Microbial Diversity of Marine Sponges |date=2003 |work=Sponges (Porifera) |pages=59–88 |editor-last=Müller |editor-first=Werner E. G. |url=https://doi.org/10.1007/978-3-642-55519-0_3 |access-date=2024-04-09 |place=Berlin, Heidelberg |publisher=Springer |language=en |doi=10.1007/978-3-642-55519-0_3 |isbn=978-3-642-55519-0 |last2=Fieseler |first2=L. |last3=Wehrl |first3=M. |last4=Gernert |first4=C. |last5=Steinert |first5=M. |last6=Hacker |first6=J. |last7=Horn |first7=M.|volume=37 |pmid=15825640 }}</ref> Shallow-water sponges in particular form complex host-microbe relationships within the marine ecosystem, with over 40 bacterial phyla identifiable on a sponge individual.<ref name=":4" /> Deep-sea sponge microbes are less diverse overall, but have more varied compositions between individual sponge organisms.<ref name=":8" /> 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. |
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Sponges can be classified as High Microbial Abundance (HMA) sponges and Low Microbial Abundance (LMA) sponges based on the density of microorganisms they host.<ref name=":13">{{Cite journal | |
Sponges can be classified as High Microbial Abundance (HMA) sponges and Low Microbial Abundance (LMA) sponges based on the density of microorganisms they host.<ref name=":13">{{Cite journal |last1=Hentschel |first1=Ute |last2=Usher |first2=Kayley M. |last3=Taylor |first3=Michael W. |date=February 2006 |title=Marine sponges as microbial fermenters |url=https://doi.org/10.1111/j.1574-6941.2005.00046.x |journal=FEMS Microbiology Ecology |volume=55 |issue=2 |pages=167–177 |doi=10.1111/j.1574-6941.2005.00046.x |pmid=16420625 |bibcode=2006FEMME..55..167H |issn=0168-6496}}</ref> HMA sponges are specifically characterized by their capacity to support a 10<sup>10</sup> cells per gram of sponge tissue, whereas LMA sponges are defined by a much lower density of 10<sup>6</sup> cells per gram of sponge tissue.<ref>{{Cite journal |last=Lesser |first=Michael P. |date=December 2023 |title=Size Effects on Pumping Rates in High Microbial versus Low Microbial Abundance Marine Sponges |journal=Oceans |language=en |volume=4 |issue=4 |pages=394–408 |doi=10.3390/oceans4040027 |doi-access=free |issn=2673-1924}}</ref> In HMA sponges, up to one third of the overall sponge biomass can be microbial biomass. <ref name=":14" /> [[Chloroflexota]], [[Gammaproteobacteria]], and [[Alphaproteobacteria]] are phyla and subphyla that have been reported to characterize HMA species.<ref>{{Cite journal |last1=Moitinho-Silva |first1=Lucas |last2=Bayer |first2=Kristina |last3=Cannistraci |first3=Carlo V. |last4=Giles |first4=Emily C. |last5=Ryu |first5=Taewoo |last6=Seridi |first6=Loqmane |last7=Ravasi |first7=Timothy |last8=Hentschel |first8=Ute |date=March 2014 |title=Specificity and transcriptional activity of microbiota associated with low and high microbial abundance sponges from the Red Sea |url=https://onlinelibrary.wiley.com/doi/10.1111/mec.12365 |journal=Molecular Ecology |language=en |volume=23 |issue=6 |pages=1348–1363 |doi=10.1111/mec.12365 |pmid=23957633 |bibcode=2014MolEc..23.1348M |issn=0962-1083}}</ref> The HMA sponge communities were found to be complex, and are dominated by [[Pseudomonadota|Proteobacteria]], [[Cyanobacteria]], [[Bacteroidota|Bacteroidetes]], [[Acidobacteriota|Acidobacteria]], and [[Planctomycetota|Planctomycetes]] in the samples from Montgri Coast (northwest [[Mediterranean Sea]]).<ref>{{Cite journal |last1=Ribes |first1=Marta |last2=Dziallas |first2=Claudia |last3=Coma |first3=Rafel |last4=Riemann |first4=Lasse |date=September 2015 |editor-last=Spormann |editor-first=A. M. |title=Microbial Diversity and Putative Diazotrophy in High- and Low-Microbial-Abundance Mediterranean Sponges |journal=Applied and Environmental Microbiology |language=en |volume=81 |issue=17 |pages=5683–5693 |doi=10.1128/AEM.01320-15 |issn=0099-2240 |pmc=4551227 |pmid=26070678|bibcode=2015ApEnM..81.5683R }}</ref> In contrast, LMA sponge communities have restricted the number of microbe species, including [[Proteobacteria]] and [[Cyanobacteria]]. <ref name=":13" /><ref name=":14">{{Cite journal |last1=Moitinho-Silva |first1=Lucas |last2=Steinert |first2=Georg |last3=Nielsen |first3=Shaun |last4=Hardoim |first4=Cristiane C. P. |last5=Wu |first5=Yu-Chen |last6=McCormack |first6=Grace P. |last7=López-Legentil |first7=Susanna |last8=Marchant |first8=Roman |last9=Webster |first9=Nicole |last10=Thomas |first10=Torsten |last11=Hentschel |first11=Ute |date=2017 |title=Predicting the HMA-LMA Status in Marine Sponges by Machine Learning |journal=Frontiers in Microbiology |volume=8 |page=752 |doi=10.3389/fmicb.2017.00752 |doi-access=free |pmid=28533766 |pmc=5421222 |issn=1664-302X}}</ref> |
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==== Symbiont Acquisition ==== |
==== Symbiont Acquisition ==== |
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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.<ref name=":7" /> The most evidenced hypothesis of sponge-specific symbionts says that sponges were colonized prior to sponge [[speciation]], during the [[Precambrian]] period.<ref>{{Cite journal |date=1984-02-22 |title=Immunological evidence for the Precambrian origin of bacterial symbioses in marine sponges |url=https://royalsocietypublishing.org/doi/10.1098/rspb.1984.0017 |journal=Proceedings of the Royal Society of London. Series B. Biological Sciences |language=en |volume=220 |issue=1221 |pages=509–518 |doi=10.1098/rspb.1984.0017 |issn=0080-4649}}</ref> This colonization is thought to have been maintained throughout the years by [[vertical transmission]], which resulted in microbial species diverging alongside sponge species.<ref name=":4" /> Support for this hypothesis comes from the presence of [[Fatty acid|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.<ref>{{Cite journal | |
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.<ref name=":7" /> The most evidenced hypothesis of sponge-specific symbionts says that sponges were colonized prior to sponge [[speciation]], during the [[Precambrian]] period.<ref>{{Cite journal |date=1984-02-22 |title=Immunological evidence for the Precambrian origin of bacterial symbioses in marine sponges |url=https://royalsocietypublishing.org/doi/10.1098/rspb.1984.0017 |journal=Proceedings of the Royal Society of London. Series B. Biological Sciences |language=en |volume=220 |issue=1221 |pages=509–518 |doi=10.1098/rspb.1984.0017 |bibcode=1984RSPSB.220..509W |issn=0080-4649 |last1=Wilkinson |first1=C. R. }}</ref> This colonization is thought to have been maintained throughout the years by [[vertical transmission]], which resulted in microbial species diverging alongside sponge species.<ref name=":4" /> Support for this hypothesis comes from the presence of [[Fatty acid|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.<ref>{{Cite journal |last1=Thiel |first1=Volker |last2=Jenisch |first2=Angela |last3=Wörheide |first3=Gert |last4=Löwenberg |first4=Antje |last5=Reitner |first5=Joachim |last6=Michaelis |first6=Walter |date=1999-01-01 |title=Mid-chain branched alkanoic acids from "living fossil" demosponges: a link to ancient sedimentary lipids? |url=https://www.sciencedirect.com/science/article/pii/S0146638098002009 |journal=Organic Geochemistry |volume=30 |issue=1 |pages=1–14 |doi=10.1016/S0146-6380(98)00200-9 |bibcode=1999OrGeo..30....1T |hdl=11858/00-1735-0000-0001-3403-F |issn=0146-6380}}</ref> However, this hypothesis is still only a hypothesis, and it requires more evidence before it (or other hypotheses of microbe acquisition) can be confirmed. |
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=== Ecological functions === |
=== Ecological functions === |
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==== Carbon Metabolism ==== |
==== Carbon Metabolism ==== |
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Marine sponges are commonly [[Heterotroph|heterotrophic]], getting their carbon from dissolved organic material or consumption of microorganisms.<ref name=":0">{{Cite journal | |
Marine sponges are commonly [[Heterotroph|heterotrophic]], getting their carbon from dissolved organic material or consumption of microorganisms.<ref name=":0">{{Cite journal |last1=Taylor |first1=Michael W. |last2=Radax |first2=Regina |last3=Steger |first3=Doris |last4=Wagner |first4=Michael |date=June 2007 |title=Sponge-associated Microorganisms: Evolution, Ecology, and Biotechnological Potential |journal=Microbiology and Molecular Biology Reviews: MMBR |volume=71 |issue=2 |pages=295–347 |doi=10.1128/MMBR.00040-06 |issn=1092-2172 |pmc=1899876 |pmid=17554047}}</ref> However, transfer of organic carbon from the microbiome to the sponge host has been demonstrated in several sponge species.<ref name=":0" /> This is most often observed in tropical sponges that carry dense communities of [[Photosynthesis|photosynthetic]] [[cyanobacteria]], which use sunlight and oxygen to produce organic carbon<ref name=":1">{{Cite journal |last1=Webster |first1=Nicole S. |last2=Thomas |first2=Torsten |date=2016-05-04 |editor-last=Dubilier |editor-first=Nicole |editor2-last=Collier |editor2-first=R. John |title=The Sponge Hologenome |journal=mBio |language=en |volume=7 |issue=2 |pages=e00135-16 |doi=10.1128/mBio.00135-16 |issn=2161-2129 |pmc=4850255 |pmid=27103626}}</ref>. Some of that organic carbon is then provided to the sponge, largely in the form of [[glycerol]].<ref name=":1" /> 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.<ref name=":1" /><ref>{{Cite journal |last=Wilkinson |first=C. R. |date=1983-01-28 |title=Net primary productivity in coral reef sponges |url=https://pubmed.ncbi.nlm.nih.gov/17815320/ |journal=Science (New York, N.Y.) |volume=219 |issue=4583 |pages=410–412 |doi=10.1126/science.219.4583.410 |issn=0036-8075 |pmid=17815320|bibcode=1983Sci...219..410W }}</ref> 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.<ref>{{Cite journal |last=Wilkinson |first=C. R. |date=1987-06-26 |title=Interocean differences in size and nutrition of coral reef sponge populations |url=https://pubmed.ncbi.nlm.nih.gov/17754318/ |journal=Science (New York, N.Y.) |volume=236 |issue=4809 |pages=1654–1657 |doi=10.1126/science.236.4809.1654 |issn=0036-8075 |pmid=17754318|bibcode=1987Sci...236.1654W }}</ref> |
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A more unusual form of carbon exchange utilizing [[methane]] has been observed in [[Carnivore|carnivorous]] deep-sea sponges (family [[Cladorhizidae]]) living near [[Hydrothermal vent|hydrothermal vents]].<ref name=":2">{{Cite journal | |
A more unusual form of carbon exchange utilizing [[methane]] has been observed in [[Carnivore|carnivorous]] deep-sea sponges (family [[Cladorhizidae]]) living near [[Hydrothermal vent|hydrothermal vents]].<ref name=":2">{{Cite journal |last1=Vacelet |first1=J. |last2=Boury-Esnault |first2=N. |date=2002 |title=A new species of carnivorous deep-sea sponge (Demospongiae: Cladorhizidae) associated with methanotrophic bacteria |journal=Cahiers de Biologie Marine|s2cid=89518839 }}</ref> The level of [[methanol dehydrogenase]] present within the sponge tissues indicates that these sponges are host to [[Methanotroph|methanotrophic]] bacteria, which thrive off of methane gas from nearby hydrothermal vents.<ref name=":3">{{Cite journal |last1=Vacelet |first1=J. |last2=FialaMedioni |first2=A. |last3=Fisher |first3=C. R. |last4=BouryEsnault |first4=N. |date=December 1996 |title=Symbiosis between methane-oxidizing bacteria and a deep-sea carnivorous cladorhizid sponge |url=https://www.webofscience.com/wos/woscc/full-record/WOS:A1996WG98200008?SID=USW2EC0A82FLFMRWdw60ySk93vNuh |journal=Marine Ecology Progress Series |language=English |volume=145 |issue=1–3 |pages=77–85 |doi=10.3354/meps145077 |bibcode=1996MEPS..145...77V |issn=0171-8630}}</ref> Instead of extracellular nutrient transfer (such as with photosynthetic cyanobacteria), most sponge cells are able to [[Phagocytosis|phagocytose]] old or dying bacterial cells, which are then used by the sponge as a source of organic carbon.<ref name=":3" /> ''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.<ref name=":2" /> |
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==== Nitrogen Metabolism ==== |
==== Nitrogen Metabolism ==== |
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Symbiotic microbes may assist sponges in the acquisition of organic nitrogen in two ways: [[nitrogen fixation]] and [[Anammox|ammonia oxidation]].<ref name=":0" /> |
Symbiotic microbes may assist sponges in the acquisition of organic nitrogen in two ways: [[nitrogen fixation]] and [[Anammox|ammonia oxidation]].<ref name=":0" /> |
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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.<ref name=":0" /><ref>{{Cite journal | |
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.<ref name=":0" /><ref>{{Cite journal |last1=Wilkinson |first1=C. R. |last2=Fay |first2=Peter |date=June 1979 |title=Nitrogen fixation in coral reef sponges with symbiotic cyanobacteria |url=https://www.nature.com/articles/279527a0 |journal=Nature |language=en |volume=279 |issue=5713 |pages=527–529 |doi=10.1038/279527a0 |bibcode=1979Natur.279..527W |issn=1476-4687}}</ref> The symbiotic bacteria pull [[Nitrogen|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.<ref name=":0" /> |
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[[File:Fmicb-07-01740-g002a extr.jpg|thumb|212x212px|''[[Methylomirabilis oxyfera]]'' ]] |
[[File:Fmicb-07-01740-g002a extr.jpg|thumb|212x212px|''[[Methylomirabilis oxyfera]]'' ]] |
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Many sponge species are inhabited by [[Nitrification|ammonia-oxidizing]] bacteria or archaea, making ammonia oxidation one of the best-studied symbiotic functions of the sponge microbiome.<ref name=":1" /> 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.<ref>{{Cite journal | |
Many sponge species are inhabited by [[Nitrification|ammonia-oxidizing]] bacteria or archaea, making ammonia oxidation one of the best-studied symbiotic functions of the sponge microbiome.<ref name=":1" /> 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.<ref>{{Cite journal |last1=Hoffmann |first1=Friederike |last2=Radax |first2=Regina |last3=Woebken |first3=Dagmar |last4=Holtappels |first4=Moritz |last5=Lavik |first5=Gaute |last6=Rapp |first6=Hans Tore |last7=Schläppy |first7=Marie-Lise |last8=Schleper |first8=Christa |last9=Kuypers |first9=Marcel M. M. |date=September 2009 |title=Complex nitrogen cycling in the sponge Geodia barretti |url=https://sfamjournals.onlinelibrary.wiley.com/doi/10.1111/j.1462-2920.2009.01944.x |journal=Environmental Microbiology |language=en |volume=11 |issue=9 |pages=2228–2243 |doi=10.1111/j.1462-2920.2009.01944.x |pmid=19453700 |bibcode=2009EnvMi..11.2228H |issn=1462-2912}}</ref> 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.<ref>{{Cite journal |last1=Hoffmann |first1=Friederike |last2=Larsen |first2=Ole |last3=Thiel |first3=Volker |last4=Rapp |first4=Hans Tore |last5=Pape |first5=Thomas |last6=Michaelis |first6=Walter |last7=Reitner |first7=Joachim |date=January 2005 |title=An Anaerobic World in Sponges |url=http://www.tandfonline.com/doi/abs/10.1080/01490450590922505 |journal=Geomicrobiology Journal |language=en |volume=22 |issue=1–2 |pages=1–10 |doi=10.1080/01490450590922505 |bibcode=2005GmbJ...22....1H |issn=0149-0451}}</ref> This is supported by the greater presence of genes related to [[denitrification]] and [[Anammox|ammonia oxidation]] in sponge microbial communities than in surrounding free-living microbes.<ref name=":1" /> 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.<ref name=":1" /> 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.<ref>{{Cite journal |last1=Ettwig |first1=Katharina F. |last2=Butler |first2=Margaret K. |last3=Le Paslier |first3=Denis |last4=Pelletier |first4=Eric |last5=Mangenot |first5=Sophie |last6=Kuypers |first6=Marcel M. M. |last7=Schreiber |first7=Frank |last8=Dutilh |first8=Bas E. |last9=Zedelius |first9=Johannes |last10=de Beer |first10=Dirk |last11=Gloerich |first11=Jolein |last12=Wessels |first12=Hans J. C. T. |last13=van Alen |first13=Theo |last14=Luesken |first14=Francisca |last15=Wu |first15=Ming L. |date=March 2010 |title=Nitrite-driven anaerobic methane oxidation by oxygenic bacteria |url=https://www.nature.com/articles/nature08883 |journal=Nature |language=en |volume=464 |issue=7288 |pages=543–548 |doi=10.1038/nature08883 |pmid=20336137 |bibcode=2010Natur.464..543E |issn=1476-4687}}</ref> |
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==== Sulfur Metabolism ==== |
==== Sulfur Metabolism ==== |
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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.<ref name=":7" /> The sponge acts as the environment in which [[Sulfur-reducing bacteria|sulfur-reducing]] and [[Sulfur oxidizing bacteria|sulfur-oxidizing]] microbes carry out a sulfur cycle.<ref>{{Cite journal | |
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.<ref name=":7" /> The sponge acts as the environment in which [[Sulfur-reducing bacteria|sulfur-reducing]] and [[Sulfur oxidizing bacteria|sulfur-oxidizing]] microbes carry out a sulfur cycle.<ref>{{Cite journal |last1=Imhoff |first1=J. F. |last2=Trüper |first2=H. G. |date=March 1976 |title=Marine sponges as habitats of anaerobic phototrophic bacteria |url=https://pubmed.ncbi.nlm.nih.gov/24233392/ |journal=Microbial Ecology |volume=3 |issue=1 |pages=1–9 |doi=10.1007/BF02011449 |issn=0095-3628 |pmid=24233392|bibcode=1976MicEc...3....1I }}</ref> This cycling likely takes place within the anaerobic zones of the sponge, as sulfur reduction is an [[Anaerobic digestion|anaerobic]] process.<ref name=":7" /> 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.<ref name=":7" /> Current research suggests that sulfur-oxidizing bacteria may also allow sponges to root in sulfur-rich [[Sediment|sediments]] that would otherwise be uninhabitable.<ref name=":7" /> |
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==== Synthesis of B Vitamins ==== |
==== Synthesis of B Vitamins ==== |
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[[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 feeder|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.<ref>{{Cite journal | |
[[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 feeder|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.<ref>{{Cite journal |last1=Liu |first1=Michael |last2=Fan |first2=Lu |last3=Zhong |first3=Ling |last4=Kjelleberg |first4=Staffan |last5=Thomas |first5=Torsten |date=2012-02-02 |title=Metaproteogenomic analysis of a community of sponge symbionts |url=https://doi.org/10.1038/ismej.2012.1 |journal=The ISME Journal |volume=6 |issue=8 |pages=1515–1525 |doi=10.1038/ismej.2012.1 |issn=1751-7362 |pmc=3400405 |pmid=22297557|bibcode=2012ISMEJ...6.1515L }}</ref><ref>{{Cite journal |title=Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis |url=https://academic.oup.com/ismej/article/4/12/1557/7588148 |access-date=2024-04-09 |journal=The ISME Journal |date=2010 |doi=10.1038/ismej.2010.74 |last1=Thomas |first1=Torsten |last2=Rusch |first2=Doug |last3=Demaere |first3=Matt Z. |last4=Yung |first4=Pui Yi |last5=Lewis |first5=Matt |last6=Halpern |first6=Aaron |last7=Heidelberg |first7=Karla B. |last8=Egan |first8=Suhelen |last9=Steinberg |first9=Peter D. |last10=Kjelleberg |first10=Staffan |volume=4 |issue=12 |pages=1557–1567 |pmid=20520651 |bibcode=2010ISMEJ...4.1557T }}</ref><ref>{{Cite journal |last1=Fan |first1=Lu |last2=Reynolds |first2=David |last3=Liu |first3=Michael |last4=Stark |first4=Manuel |last5=Kjelleberg |first5=Staffan |last6=Webster |first6=Nicole S. |last7=Thomas |first7=Torsten |date=2012-07-03 |title=Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts |journal=Proceedings of the National Academy of Sciences |language=en |volume=109 |issue=27 |pages=E1878-87 |doi=10.1073/pnas.1203287109 |doi-access=free |issn=0027-8424 |pmc=3390844 |pmid=22699508}}</ref><ref name=":12" /> 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 [[Vitamin B12|cobalamin]] (B12).<ref name=":12">{{Cite journal |last1=Engelberts |first1=J. Pamela |last2=Robbins |first2=Steven J. |last3=de Goeij |first3=Jasper M. |last4=Aranda |first4=Manuel |last5=Bell |first5=Sara C. |last6=Webster |first6=Nicole S. |date=May 2020 |title=Characterization of a sponge microbiome using an integrative genome-centric approach |journal=The ISME Journal |volume=14 |issue=5 |pages=1100–1110 |doi=10.1038/s41396-020-0591-9 |issn=1751-7362 |pmc=7174397 |pmid=31992859|bibcode=2020ISMEJ..14.1100E }}</ref> |
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= References = |
= References = |
Revision as of 21:46, 14 April 2024
Sponge microbiomes
Overview
Sponges (Phylum Porifera) are multicellular heterotrophic marine organisms without true organs or a nervous system.[1] They are early-diverging metazoans that are known to form symbiotic relationships with complex communities of microorganisms, and are a key part of most benthic marine ecosystems where they can metabolize fundamental resources such as carbon, nitrogen, and sulfur.[1]
![](http://upload.wikimedia.org/wikipedia/commons/thumb/6/6b/The_sponge_holobiont.webp/217px-The_sponge_holobiont.webp.png)
Sponge microbiomes are diverse communities of microorganisms in symbiotic association with marine sponges as their hosts.[3] These microorganisms include bacteria, archaea, fungi, viruses, among others.[4] 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.[4][5] 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.[3][6][7] Furthermore, individual holobionts work hand in hand with other near holobionts becoming a nested ecosystem, affecting the environment at multiple scales.[4]
Composition
Microbiome Species Diversity
![](http://upload.wikimedia.org/wikipedia/commons/thumb/6/67/Taxonnomic_profile_of_microbial_communities.jpg/366px-Taxonnomic_profile_of_microbial_communities.jpg)
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.[9] Shallow-water sponges in particular form complex host-microbe relationships within the marine ecosystem, with over 40 bacterial phyla identifiable on a sponge individual.[3] Deep-sea sponge microbes are less diverse overall, but have more varied compositions between individual sponge organisms.[6] 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.[10] 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.[11] In HMA sponges, up to one third of the overall sponge biomass can be microbial biomass. [12] Chloroflexota, Gammaproteobacteria, and Alphaproteobacteria are phyla and subphyla that have been reported to characterize HMA species.[13] 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).[14] In contrast, LMA sponge communities have restricted the number of microbe species, including Proteobacteria and Cyanobacteria. [10][12]
Symbiont Acquisition
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.[1] 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.[3] 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
Carbon Metabolism
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
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]
![](http://upload.wikimedia.org/wikipedia/commons/thumb/2/28/Fmicb-07-01740-g002a_extr.jpg/212px-Fmicb-07-01740-g002a_extr.jpg)
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
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.[1] 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.[1] 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.[1] Current research suggests that sulfur-oxidizing bacteria may also allow sponges to root in sulfur-rich sediments that would otherwise be uninhabitable.[1]
Synthesis of B Vitamins
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][31] 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).[31]
References
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- ^ 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.
- ^ 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.
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- ^ 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.
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