Holobiont nitrogen control and its potential for eutrophication resistance in an obligate photosymbiotic jellyfish
Abstract Background Marine holobionts depend on microbial members for health and nutrient cycling. This is particularly evident in cnidarian-algae symbioses that facilitate energy and nutrient acquisition. However, this partnership is highly sensitive to environmental change—including eutrophication...
Ausführliche Beschreibung
Autor*in: |
Till Röthig [verfasserIn] Giulia Puntin [verfasserIn] Jane C. Y. Wong [verfasserIn] Alfred Burian [verfasserIn] Wendy McLeod [verfasserIn] David M. Baker [verfasserIn] |
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E-Artikel |
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Sprache: |
Englisch |
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2021 |
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In: Microbiome - BMC, 2013, 9(2021), 1, Seite 16 |
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Übergeordnetes Werk: |
volume:9 ; year:2021 ; number:1 ; pages:16 |
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DOI / URN: |
10.1186/s40168-021-01075-0 |
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Katalog-ID: |
DOAJ005423384 |
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520 | |a Abstract Background Marine holobionts depend on microbial members for health and nutrient cycling. This is particularly evident in cnidarian-algae symbioses that facilitate energy and nutrient acquisition. However, this partnership is highly sensitive to environmental change—including eutrophication—that causes dysbiosis and contributes to global coral reef decline. Yet, some holobionts exhibit resistance to dysbiosis in eutrophic environments, including the obligate photosymbiotic scyphomedusa Cassiopea xamachana. Methods Our aim was to assess the mechanisms in C. xamachana that stabilize symbiotic relationships. We combined labelled bicarbonate (13C) and nitrate (15N) with metabarcoding approaches to evaluate nutrient cycling and microbial community composition in symbiotic and aposymbiotic medusae. Results C-fixation and cycling by algal Symbiodiniaceae was essential for C. xamachana as even at high heterotrophic feeding rates aposymbiotic medusae continuously lost weight. Heterotrophically acquired C and N were readily shared among host and algae. This was in sharp contrast to nitrate assimilation by Symbiodiniaceae, which appeared to be strongly restricted. Instead, the bacterial microbiome seemed to play a major role in the holobiont’s DIN assimilation as uptake rates showed a significant positive relationship with phylogenetic diversity of medusa-associated bacteria. This is corroborated by inferred functional capacity that links the dominant bacterial taxa (~90 %) to nitrogen cycling. Observed bacterial community structure differed between apo- and symbiotic C. xamachana putatively highlighting enrichment of ammonium oxidizers and nitrite reducers and depletion of nitrogen-fixers in symbiotic medusae. Conclusion Host, algal symbionts, and bacterial associates contribute to regulated nutrient assimilation and cycling in C. xamachana. We found that the bacterial microbiome of symbiotic medusae was seemingly structured to increase DIN removal and enforce algal N-limitation—a mechanism that would help to stabilize the host-algae relationship even under eutrophic conditions. Video abstract | ||
650 | 4 | |a Stable isotope analysis | |
650 | 4 | |a Tracer | |
650 | 4 | |a Bacterial profiling | |
650 | 4 | |a Environmental resilience | |
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653 | 0 | |a Microbial ecology | |
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700 | 0 | |a Jane C. Y. Wong |e verfasserin |4 aut | |
700 | 0 | |a Alfred Burian |e verfasserin |4 aut | |
700 | 0 | |a Wendy McLeod |e verfasserin |4 aut | |
700 | 0 | |a David M. Baker |e verfasserin |4 aut | |
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10.1186/s40168-021-01075-0 doi (DE-627)DOAJ005423384 (DE-599)DOAJ1bd4d44e528445a6bab2d96a8f89a89e DE-627 ger DE-627 rakwb eng QR100-130 Till Röthig verfasserin aut Holobiont nitrogen control and its potential for eutrophication resistance in an obligate photosymbiotic jellyfish 2021 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier Abstract Background Marine holobionts depend on microbial members for health and nutrient cycling. This is particularly evident in cnidarian-algae symbioses that facilitate energy and nutrient acquisition. However, this partnership is highly sensitive to environmental change—including eutrophication—that causes dysbiosis and contributes to global coral reef decline. Yet, some holobionts exhibit resistance to dysbiosis in eutrophic environments, including the obligate photosymbiotic scyphomedusa Cassiopea xamachana. Methods Our aim was to assess the mechanisms in C. xamachana that stabilize symbiotic relationships. We combined labelled bicarbonate (13C) and nitrate (15N) with metabarcoding approaches to evaluate nutrient cycling and microbial community composition in symbiotic and aposymbiotic medusae. Results C-fixation and cycling by algal Symbiodiniaceae was essential for C. xamachana as even at high heterotrophic feeding rates aposymbiotic medusae continuously lost weight. Heterotrophically acquired C and N were readily shared among host and algae. This was in sharp contrast to nitrate assimilation by Symbiodiniaceae, which appeared to be strongly restricted. Instead, the bacterial microbiome seemed to play a major role in the holobiont’s DIN assimilation as uptake rates showed a significant positive relationship with phylogenetic diversity of medusa-associated bacteria. This is corroborated by inferred functional capacity that links the dominant bacterial taxa (~90 %) to nitrogen cycling. Observed bacterial community structure differed between apo- and symbiotic C. xamachana putatively highlighting enrichment of ammonium oxidizers and nitrite reducers and depletion of nitrogen-fixers in symbiotic medusae. Conclusion Host, algal symbionts, and bacterial associates contribute to regulated nutrient assimilation and cycling in C. xamachana. We found that the bacterial microbiome of symbiotic medusae was seemingly structured to increase DIN removal and enforce algal N-limitation—a mechanism that would help to stabilize the host-algae relationship even under eutrophic conditions. Video abstract Stable isotope analysis Tracer Bacterial profiling Environmental resilience 16S rRNA gene Microbial ecology Giulia Puntin verfasserin aut Jane C. Y. Wong verfasserin aut Alfred Burian verfasserin aut Wendy McLeod verfasserin aut David M. Baker verfasserin aut In Microbiome BMC, 2013 9(2021), 1, Seite 16 (DE-627)734146140 (DE-600)2697425-3 20492618 nnns volume:9 year:2021 number:1 pages:16 https://doi.org/10.1186/s40168-021-01075-0 kostenfrei https://doaj.org/article/1bd4d44e528445a6bab2d96a8f89a89e kostenfrei https://doi.org/10.1186/s40168-021-01075-0 kostenfrei https://doaj.org/toc/2049-2618 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ SSG-OLC-PHA GBV_ILN_11 GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2003 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 9 2021 1 16 |
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10.1186/s40168-021-01075-0 doi (DE-627)DOAJ005423384 (DE-599)DOAJ1bd4d44e528445a6bab2d96a8f89a89e DE-627 ger DE-627 rakwb eng QR100-130 Till Röthig verfasserin aut Holobiont nitrogen control and its potential for eutrophication resistance in an obligate photosymbiotic jellyfish 2021 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier Abstract Background Marine holobionts depend on microbial members for health and nutrient cycling. This is particularly evident in cnidarian-algae symbioses that facilitate energy and nutrient acquisition. However, this partnership is highly sensitive to environmental change—including eutrophication—that causes dysbiosis and contributes to global coral reef decline. Yet, some holobionts exhibit resistance to dysbiosis in eutrophic environments, including the obligate photosymbiotic scyphomedusa Cassiopea xamachana. Methods Our aim was to assess the mechanisms in C. xamachana that stabilize symbiotic relationships. We combined labelled bicarbonate (13C) and nitrate (15N) with metabarcoding approaches to evaluate nutrient cycling and microbial community composition in symbiotic and aposymbiotic medusae. Results C-fixation and cycling by algal Symbiodiniaceae was essential for C. xamachana as even at high heterotrophic feeding rates aposymbiotic medusae continuously lost weight. Heterotrophically acquired C and N were readily shared among host and algae. This was in sharp contrast to nitrate assimilation by Symbiodiniaceae, which appeared to be strongly restricted. Instead, the bacterial microbiome seemed to play a major role in the holobiont’s DIN assimilation as uptake rates showed a significant positive relationship with phylogenetic diversity of medusa-associated bacteria. This is corroborated by inferred functional capacity that links the dominant bacterial taxa (~90 %) to nitrogen cycling. Observed bacterial community structure differed between apo- and symbiotic C. xamachana putatively highlighting enrichment of ammonium oxidizers and nitrite reducers and depletion of nitrogen-fixers in symbiotic medusae. Conclusion Host, algal symbionts, and bacterial associates contribute to regulated nutrient assimilation and cycling in C. xamachana. We found that the bacterial microbiome of symbiotic medusae was seemingly structured to increase DIN removal and enforce algal N-limitation—a mechanism that would help to stabilize the host-algae relationship even under eutrophic conditions. Video abstract Stable isotope analysis Tracer Bacterial profiling Environmental resilience 16S rRNA gene Microbial ecology Giulia Puntin verfasserin aut Jane C. Y. Wong verfasserin aut Alfred Burian verfasserin aut Wendy McLeod verfasserin aut David M. Baker verfasserin aut In Microbiome BMC, 2013 9(2021), 1, Seite 16 (DE-627)734146140 (DE-600)2697425-3 20492618 nnns volume:9 year:2021 number:1 pages:16 https://doi.org/10.1186/s40168-021-01075-0 kostenfrei https://doaj.org/article/1bd4d44e528445a6bab2d96a8f89a89e kostenfrei https://doi.org/10.1186/s40168-021-01075-0 kostenfrei https://doaj.org/toc/2049-2618 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ SSG-OLC-PHA GBV_ILN_11 GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2003 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 9 2021 1 16 |
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10.1186/s40168-021-01075-0 doi (DE-627)DOAJ005423384 (DE-599)DOAJ1bd4d44e528445a6bab2d96a8f89a89e DE-627 ger DE-627 rakwb eng QR100-130 Till Röthig verfasserin aut Holobiont nitrogen control and its potential for eutrophication resistance in an obligate photosymbiotic jellyfish 2021 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier Abstract Background Marine holobionts depend on microbial members for health and nutrient cycling. This is particularly evident in cnidarian-algae symbioses that facilitate energy and nutrient acquisition. However, this partnership is highly sensitive to environmental change—including eutrophication—that causes dysbiosis and contributes to global coral reef decline. Yet, some holobionts exhibit resistance to dysbiosis in eutrophic environments, including the obligate photosymbiotic scyphomedusa Cassiopea xamachana. Methods Our aim was to assess the mechanisms in C. xamachana that stabilize symbiotic relationships. We combined labelled bicarbonate (13C) and nitrate (15N) with metabarcoding approaches to evaluate nutrient cycling and microbial community composition in symbiotic and aposymbiotic medusae. Results C-fixation and cycling by algal Symbiodiniaceae was essential for C. xamachana as even at high heterotrophic feeding rates aposymbiotic medusae continuously lost weight. Heterotrophically acquired C and N were readily shared among host and algae. This was in sharp contrast to nitrate assimilation by Symbiodiniaceae, which appeared to be strongly restricted. Instead, the bacterial microbiome seemed to play a major role in the holobiont’s DIN assimilation as uptake rates showed a significant positive relationship with phylogenetic diversity of medusa-associated bacteria. This is corroborated by inferred functional capacity that links the dominant bacterial taxa (~90 %) to nitrogen cycling. Observed bacterial community structure differed between apo- and symbiotic C. xamachana putatively highlighting enrichment of ammonium oxidizers and nitrite reducers and depletion of nitrogen-fixers in symbiotic medusae. Conclusion Host, algal symbionts, and bacterial associates contribute to regulated nutrient assimilation and cycling in C. xamachana. We found that the bacterial microbiome of symbiotic medusae was seemingly structured to increase DIN removal and enforce algal N-limitation—a mechanism that would help to stabilize the host-algae relationship even under eutrophic conditions. Video abstract Stable isotope analysis Tracer Bacterial profiling Environmental resilience 16S rRNA gene Microbial ecology Giulia Puntin verfasserin aut Jane C. Y. Wong verfasserin aut Alfred Burian verfasserin aut Wendy McLeod verfasserin aut David M. Baker verfasserin aut In Microbiome BMC, 2013 9(2021), 1, Seite 16 (DE-627)734146140 (DE-600)2697425-3 20492618 nnns volume:9 year:2021 number:1 pages:16 https://doi.org/10.1186/s40168-021-01075-0 kostenfrei https://doaj.org/article/1bd4d44e528445a6bab2d96a8f89a89e kostenfrei https://doi.org/10.1186/s40168-021-01075-0 kostenfrei https://doaj.org/toc/2049-2618 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ SSG-OLC-PHA GBV_ILN_11 GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2003 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 9 2021 1 16 |
allfieldsGer |
10.1186/s40168-021-01075-0 doi (DE-627)DOAJ005423384 (DE-599)DOAJ1bd4d44e528445a6bab2d96a8f89a89e DE-627 ger DE-627 rakwb eng QR100-130 Till Röthig verfasserin aut Holobiont nitrogen control and its potential for eutrophication resistance in an obligate photosymbiotic jellyfish 2021 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier Abstract Background Marine holobionts depend on microbial members for health and nutrient cycling. This is particularly evident in cnidarian-algae symbioses that facilitate energy and nutrient acquisition. However, this partnership is highly sensitive to environmental change—including eutrophication—that causes dysbiosis and contributes to global coral reef decline. Yet, some holobionts exhibit resistance to dysbiosis in eutrophic environments, including the obligate photosymbiotic scyphomedusa Cassiopea xamachana. Methods Our aim was to assess the mechanisms in C. xamachana that stabilize symbiotic relationships. We combined labelled bicarbonate (13C) and nitrate (15N) with metabarcoding approaches to evaluate nutrient cycling and microbial community composition in symbiotic and aposymbiotic medusae. Results C-fixation and cycling by algal Symbiodiniaceae was essential for C. xamachana as even at high heterotrophic feeding rates aposymbiotic medusae continuously lost weight. Heterotrophically acquired C and N were readily shared among host and algae. This was in sharp contrast to nitrate assimilation by Symbiodiniaceae, which appeared to be strongly restricted. Instead, the bacterial microbiome seemed to play a major role in the holobiont’s DIN assimilation as uptake rates showed a significant positive relationship with phylogenetic diversity of medusa-associated bacteria. This is corroborated by inferred functional capacity that links the dominant bacterial taxa (~90 %) to nitrogen cycling. Observed bacterial community structure differed between apo- and symbiotic C. xamachana putatively highlighting enrichment of ammonium oxidizers and nitrite reducers and depletion of nitrogen-fixers in symbiotic medusae. Conclusion Host, algal symbionts, and bacterial associates contribute to regulated nutrient assimilation and cycling in C. xamachana. We found that the bacterial microbiome of symbiotic medusae was seemingly structured to increase DIN removal and enforce algal N-limitation—a mechanism that would help to stabilize the host-algae relationship even under eutrophic conditions. Video abstract Stable isotope analysis Tracer Bacterial profiling Environmental resilience 16S rRNA gene Microbial ecology Giulia Puntin verfasserin aut Jane C. Y. Wong verfasserin aut Alfred Burian verfasserin aut Wendy McLeod verfasserin aut David M. Baker verfasserin aut In Microbiome BMC, 2013 9(2021), 1, Seite 16 (DE-627)734146140 (DE-600)2697425-3 20492618 nnns volume:9 year:2021 number:1 pages:16 https://doi.org/10.1186/s40168-021-01075-0 kostenfrei https://doaj.org/article/1bd4d44e528445a6bab2d96a8f89a89e kostenfrei https://doi.org/10.1186/s40168-021-01075-0 kostenfrei https://doaj.org/toc/2049-2618 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ SSG-OLC-PHA GBV_ILN_11 GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2003 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 9 2021 1 16 |
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10.1186/s40168-021-01075-0 doi (DE-627)DOAJ005423384 (DE-599)DOAJ1bd4d44e528445a6bab2d96a8f89a89e DE-627 ger DE-627 rakwb eng QR100-130 Till Röthig verfasserin aut Holobiont nitrogen control and its potential for eutrophication resistance in an obligate photosymbiotic jellyfish 2021 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier Abstract Background Marine holobionts depend on microbial members for health and nutrient cycling. This is particularly evident in cnidarian-algae symbioses that facilitate energy and nutrient acquisition. However, this partnership is highly sensitive to environmental change—including eutrophication—that causes dysbiosis and contributes to global coral reef decline. Yet, some holobionts exhibit resistance to dysbiosis in eutrophic environments, including the obligate photosymbiotic scyphomedusa Cassiopea xamachana. Methods Our aim was to assess the mechanisms in C. xamachana that stabilize symbiotic relationships. We combined labelled bicarbonate (13C) and nitrate (15N) with metabarcoding approaches to evaluate nutrient cycling and microbial community composition in symbiotic and aposymbiotic medusae. Results C-fixation and cycling by algal Symbiodiniaceae was essential for C. xamachana as even at high heterotrophic feeding rates aposymbiotic medusae continuously lost weight. Heterotrophically acquired C and N were readily shared among host and algae. This was in sharp contrast to nitrate assimilation by Symbiodiniaceae, which appeared to be strongly restricted. Instead, the bacterial microbiome seemed to play a major role in the holobiont’s DIN assimilation as uptake rates showed a significant positive relationship with phylogenetic diversity of medusa-associated bacteria. This is corroborated by inferred functional capacity that links the dominant bacterial taxa (~90 %) to nitrogen cycling. Observed bacterial community structure differed between apo- and symbiotic C. xamachana putatively highlighting enrichment of ammonium oxidizers and nitrite reducers and depletion of nitrogen-fixers in symbiotic medusae. Conclusion Host, algal symbionts, and bacterial associates contribute to regulated nutrient assimilation and cycling in C. xamachana. We found that the bacterial microbiome of symbiotic medusae was seemingly structured to increase DIN removal and enforce algal N-limitation—a mechanism that would help to stabilize the host-algae relationship even under eutrophic conditions. Video abstract Stable isotope analysis Tracer Bacterial profiling Environmental resilience 16S rRNA gene Microbial ecology Giulia Puntin verfasserin aut Jane C. Y. Wong verfasserin aut Alfred Burian verfasserin aut Wendy McLeod verfasserin aut David M. Baker verfasserin aut In Microbiome BMC, 2013 9(2021), 1, Seite 16 (DE-627)734146140 (DE-600)2697425-3 20492618 nnns volume:9 year:2021 number:1 pages:16 https://doi.org/10.1186/s40168-021-01075-0 kostenfrei https://doaj.org/article/1bd4d44e528445a6bab2d96a8f89a89e kostenfrei https://doi.org/10.1186/s40168-021-01075-0 kostenfrei https://doaj.org/toc/2049-2618 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ SSG-OLC-PHA GBV_ILN_11 GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2003 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 9 2021 1 16 |
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Abstract Background Marine holobionts depend on microbial members for health and nutrient cycling. This is particularly evident in cnidarian-algae symbioses that facilitate energy and nutrient acquisition. However, this partnership is highly sensitive to environmental change—including eutrophication—that causes dysbiosis and contributes to global coral reef decline. Yet, some holobionts exhibit resistance to dysbiosis in eutrophic environments, including the obligate photosymbiotic scyphomedusa Cassiopea xamachana. Methods Our aim was to assess the mechanisms in C. xamachana that stabilize symbiotic relationships. We combined labelled bicarbonate (13C) and nitrate (15N) with metabarcoding approaches to evaluate nutrient cycling and microbial community composition in symbiotic and aposymbiotic medusae. Results C-fixation and cycling by algal Symbiodiniaceae was essential for C. xamachana as even at high heterotrophic feeding rates aposymbiotic medusae continuously lost weight. Heterotrophically acquired C and N were readily shared among host and algae. This was in sharp contrast to nitrate assimilation by Symbiodiniaceae, which appeared to be strongly restricted. Instead, the bacterial microbiome seemed to play a major role in the holobiont’s DIN assimilation as uptake rates showed a significant positive relationship with phylogenetic diversity of medusa-associated bacteria. This is corroborated by inferred functional capacity that links the dominant bacterial taxa (~90 %) to nitrogen cycling. Observed bacterial community structure differed between apo- and symbiotic C. xamachana putatively highlighting enrichment of ammonium oxidizers and nitrite reducers and depletion of nitrogen-fixers in symbiotic medusae. Conclusion Host, algal symbionts, and bacterial associates contribute to regulated nutrient assimilation and cycling in C. xamachana. We found that the bacterial microbiome of symbiotic medusae was seemingly structured to increase DIN removal and enforce algal N-limitation—a mechanism that would help to stabilize the host-algae relationship even under eutrophic conditions. Video abstract |
abstractGer |
Abstract Background Marine holobionts depend on microbial members for health and nutrient cycling. This is particularly evident in cnidarian-algae symbioses that facilitate energy and nutrient acquisition. However, this partnership is highly sensitive to environmental change—including eutrophication—that causes dysbiosis and contributes to global coral reef decline. Yet, some holobionts exhibit resistance to dysbiosis in eutrophic environments, including the obligate photosymbiotic scyphomedusa Cassiopea xamachana. Methods Our aim was to assess the mechanisms in C. xamachana that stabilize symbiotic relationships. We combined labelled bicarbonate (13C) and nitrate (15N) with metabarcoding approaches to evaluate nutrient cycling and microbial community composition in symbiotic and aposymbiotic medusae. Results C-fixation and cycling by algal Symbiodiniaceae was essential for C. xamachana as even at high heterotrophic feeding rates aposymbiotic medusae continuously lost weight. Heterotrophically acquired C and N were readily shared among host and algae. This was in sharp contrast to nitrate assimilation by Symbiodiniaceae, which appeared to be strongly restricted. Instead, the bacterial microbiome seemed to play a major role in the holobiont’s DIN assimilation as uptake rates showed a significant positive relationship with phylogenetic diversity of medusa-associated bacteria. This is corroborated by inferred functional capacity that links the dominant bacterial taxa (~90 %) to nitrogen cycling. Observed bacterial community structure differed between apo- and symbiotic C. xamachana putatively highlighting enrichment of ammonium oxidizers and nitrite reducers and depletion of nitrogen-fixers in symbiotic medusae. Conclusion Host, algal symbionts, and bacterial associates contribute to regulated nutrient assimilation and cycling in C. xamachana. We found that the bacterial microbiome of symbiotic medusae was seemingly structured to increase DIN removal and enforce algal N-limitation—a mechanism that would help to stabilize the host-algae relationship even under eutrophic conditions. Video abstract |
abstract_unstemmed |
Abstract Background Marine holobionts depend on microbial members for health and nutrient cycling. This is particularly evident in cnidarian-algae symbioses that facilitate energy and nutrient acquisition. However, this partnership is highly sensitive to environmental change—including eutrophication—that causes dysbiosis and contributes to global coral reef decline. Yet, some holobionts exhibit resistance to dysbiosis in eutrophic environments, including the obligate photosymbiotic scyphomedusa Cassiopea xamachana. Methods Our aim was to assess the mechanisms in C. xamachana that stabilize symbiotic relationships. We combined labelled bicarbonate (13C) and nitrate (15N) with metabarcoding approaches to evaluate nutrient cycling and microbial community composition in symbiotic and aposymbiotic medusae. Results C-fixation and cycling by algal Symbiodiniaceae was essential for C. xamachana as even at high heterotrophic feeding rates aposymbiotic medusae continuously lost weight. Heterotrophically acquired C and N were readily shared among host and algae. This was in sharp contrast to nitrate assimilation by Symbiodiniaceae, which appeared to be strongly restricted. Instead, the bacterial microbiome seemed to play a major role in the holobiont’s DIN assimilation as uptake rates showed a significant positive relationship with phylogenetic diversity of medusa-associated bacteria. This is corroborated by inferred functional capacity that links the dominant bacterial taxa (~90 %) to nitrogen cycling. Observed bacterial community structure differed between apo- and symbiotic C. xamachana putatively highlighting enrichment of ammonium oxidizers and nitrite reducers and depletion of nitrogen-fixers in symbiotic medusae. Conclusion Host, algal symbionts, and bacterial associates contribute to regulated nutrient assimilation and cycling in C. xamachana. We found that the bacterial microbiome of symbiotic medusae was seemingly structured to increase DIN removal and enforce algal N-limitation—a mechanism that would help to stabilize the host-algae relationship even under eutrophic conditions. Video abstract |
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Holobiont nitrogen control and its potential for eutrophication resistance in an obligate photosymbiotic jellyfish |
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https://doi.org/10.1186/s40168-021-01075-0 https://doaj.org/article/1bd4d44e528445a6bab2d96a8f89a89e https://doaj.org/toc/2049-2618 |
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Giulia Puntin Jane C. Y. Wong Alfred Burian Wendy McLeod David M. Baker |
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