Assessing the effects of iron enrichment across holobiont compartments reveals reduced microbial nitrogen fixation in the Red Sea coral Pocillopora verrucosa

Handle URI:
http://hdl.handle.net/10754/625310
Title:
Assessing the effects of iron enrichment across holobiont compartments reveals reduced microbial nitrogen fixation in the Red Sea coral Pocillopora verrucosa
Authors:
Radecker, Nils; Pogoreutz, Claudia; Ziegler, Maren ( 0000-0003-2237-9261 ) ; Ashok, Ananya; Barreto, Marcelle M.; Chaidez, Veronica ( 0000-0003-1340-5835 ) ; Grupstra, Carsten G. B.; Ng, Yi Mei; Perna, Gabriela; Aranda, Manuel ( 0000-0001-6673-016X ) ; Voolstra, Christian R. ( 0000-0003-4555-3795 )
Abstract:
The productivity of coral reefs in oligotrophic tropical waters is sustained by an efficient uptake and recycling of nutrients. In reef-building corals, the engineers of these ecosystems, this nutrient recycling is facilitated by a constant exchange of nutrients between the animal host and endosymbiotic photosynthetic dinoflagellates (zooxanthellae), bacteria, and other microbes. Due to the complex interactions in this so-called coral holobiont, it has proven difficult to understand the environmental limitations of productivity in corals. Among others, the micronutrient iron has been proposed to limit primary productivity due to its essential role in photosynthesis and bacterial processes. Here, we tested the effect of iron enrichment on the physiology of the coral Pocillopora verrucosa from the central Red Sea during a 12-day experiment. Contrary to previous reports, we did not see an increase in zooxanthellae population density or gross photosynthesis. Conversely, respiration rates were significantly increased, and microbial nitrogen fixation was significantly decreased. Taken together, our data suggest that iron is not a limiting factor of primary productivity in Red Sea corals. Rather, increased metabolic demands in response to iron enrichment, as evidenced by increased respiration rates, may reduce carbon (i.e., energy) availability in the coral holobiont, resulting in reduced microbial nitrogen fixation. This decrease in nitrogen supply in turn may exacerbate the limitation of other nutrients, creating a negative feedback loop. Thereby, our results highlight that the effects of iron enrichment appear to be strongly dependent on local environmental conditions and ultimately may depend on the availability of other nutrients.
KAUST Department:
Biological and Environmental Sciences and Engineering (BESE) Division; Red Sea Research Center (RSRC)
Citation:
Rädecker N, Pogoreutz C, Ziegler M, Ashok A, Barreto MM, et al. (2017) Assessing the effects of iron enrichment across holobiont compartments reveals reduced microbial nitrogen fixation in the Red Sea coral Pocillopora verrucosa . Ecology and Evolution. Available: http://dx.doi.org/10.1002/ece3.3293.
Publisher:
Wiley-Blackwell
Journal:
Ecology and Evolution
Issue Date:
31-Jul-2017
DOI:
10.1002/ece3.3293
Type:
Article
ISSN:
2045-7758
Sponsors:
We thank Paul Müller and Zenon Batang for allocation of laboratory space at CMOR and for their assistance with the aquaria set up and maintenance. Further, we thank Alaguraj Dharmarajnadar for his help with flow cytometry and data analysis. CRV acknowledges funding by the King Abdullah University of Science and Technology (KAUST). This experiment was conducted as part of the Marine Science MarS330 course “Ecological Genomics.” We would also like to thank the editor and three anonymous reviewers for their valuable feedback on our manuscript.
Additional Links:
http://onlinelibrary.wiley.com/doi/10.1002/ece3.3293/full
Appears in Collections:
Articles; Red Sea Research Center (RSRC); Biological and Environmental Sciences and Engineering (BESE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorRadecker, Nilsen
dc.contributor.authorPogoreutz, Claudiaen
dc.contributor.authorZiegler, Marenen
dc.contributor.authorAshok, Ananyaen
dc.contributor.authorBarreto, Marcelle M.en
dc.contributor.authorChaidez, Veronicaen
dc.contributor.authorGrupstra, Carsten G. B.en
dc.contributor.authorNg, Yi Meien
dc.contributor.authorPerna, Gabrielaen
dc.contributor.authorAranda, Manuelen
dc.contributor.authorVoolstra, Christian R.en
dc.date.accessioned2017-08-10T11:43:32Z-
dc.date.available2017-08-10T11:43:32Z-
dc.date.issued2017-07-31en
dc.identifier.citationRädecker N, Pogoreutz C, Ziegler M, Ashok A, Barreto MM, et al. (2017) Assessing the effects of iron enrichment across holobiont compartments reveals reduced microbial nitrogen fixation in the Red Sea coral Pocillopora verrucosa . Ecology and Evolution. Available: http://dx.doi.org/10.1002/ece3.3293.en
dc.identifier.issn2045-7758en
dc.identifier.doi10.1002/ece3.3293en
dc.identifier.urihttp://hdl.handle.net/10754/625310-
dc.description.abstractThe productivity of coral reefs in oligotrophic tropical waters is sustained by an efficient uptake and recycling of nutrients. In reef-building corals, the engineers of these ecosystems, this nutrient recycling is facilitated by a constant exchange of nutrients between the animal host and endosymbiotic photosynthetic dinoflagellates (zooxanthellae), bacteria, and other microbes. Due to the complex interactions in this so-called coral holobiont, it has proven difficult to understand the environmental limitations of productivity in corals. Among others, the micronutrient iron has been proposed to limit primary productivity due to its essential role in photosynthesis and bacterial processes. Here, we tested the effect of iron enrichment on the physiology of the coral Pocillopora verrucosa from the central Red Sea during a 12-day experiment. Contrary to previous reports, we did not see an increase in zooxanthellae population density or gross photosynthesis. Conversely, respiration rates were significantly increased, and microbial nitrogen fixation was significantly decreased. Taken together, our data suggest that iron is not a limiting factor of primary productivity in Red Sea corals. Rather, increased metabolic demands in response to iron enrichment, as evidenced by increased respiration rates, may reduce carbon (i.e., energy) availability in the coral holobiont, resulting in reduced microbial nitrogen fixation. This decrease in nitrogen supply in turn may exacerbate the limitation of other nutrients, creating a negative feedback loop. Thereby, our results highlight that the effects of iron enrichment appear to be strongly dependent on local environmental conditions and ultimately may depend on the availability of other nutrients.en
dc.description.sponsorshipWe thank Paul Müller and Zenon Batang for allocation of laboratory space at CMOR and for their assistance with the aquaria set up and maintenance. Further, we thank Alaguraj Dharmarajnadar for his help with flow cytometry and data analysis. CRV acknowledges funding by the King Abdullah University of Science and Technology (KAUST). This experiment was conducted as part of the Marine Science MarS330 course “Ecological Genomics.” We would also like to thank the editor and three anonymous reviewers for their valuable feedback on our manuscript.en
dc.publisherWiley-Blackwellen
dc.relation.urlhttp://onlinelibrary.wiley.com/doi/10.1002/ece3.3293/fullen
dc.rightsThis is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.en
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/en
dc.subjectSymbiodiniumen
dc.subjectCoral reefsen
dc.subjectDiazotrophen
dc.subjectHolobionten
dc.subjectNutrient limitationen
dc.subjectSymbiosisen
dc.titleAssessing the effects of iron enrichment across holobiont compartments reveals reduced microbial nitrogen fixation in the Red Sea coral Pocillopora verrucosaen
dc.typeArticleen
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.contributor.departmentRed Sea Research Center (RSRC)en
dc.identifier.journalEcology and Evolutionen
dc.eprint.versionPublisher's Version/PDFen
kaust.authorRadecker, Nilsen
kaust.authorPogoreutz, Claudiaen
kaust.authorZiegler, Marenen
kaust.authorAshok, Ananyaen
kaust.authorBarreto, Marcelle M.en
kaust.authorChaidez, Veronicaen
kaust.authorGrupstra, Carsten G. B.en
kaust.authorNg, Yi Meien
kaust.authorPerna, Gabrielaen
kaust.authorAranda, Manuelen
kaust.authorVoolstra, Christian R.en
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