Gabriela Perna

University of Konstanz

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Christian R. Voolstra

University of Konstanz

Anny Cárdenas

University of Konstanz

Nils Rädecker

École Polytechnique Fédérale de Lausanne

Claudia Pogoreutz

University of Konstanz

Mathieu Pernice

University of Technology Sydney

Benjamin C. C. Hume

University of Konstanz

Paul Guagliardo

University of Western Australia

Rupert Ormond

Heriot-Watt University

Daniel J. Barshis

Old Dominion University

Mauvis Gore

Heriot-Watt University

Cooperative Institutions

Centre National de la Recherche Scientifique

Genoscope

Commissariat à l'Énergie Atomique et aux Énergies Alternatives

Université Paris-Saclay

CEA Paris-Saclay

King Abdullah University of Science and Technology

University of Konstanz

Weizmann Institute of Science

Universidade Federal do Rio de Janeiro

Université d'Évry Val-d'Essonne

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Coral holobiont cues prime Endozoicomonas for a symbiotic lifestyle

The ISME Journal (2022)

Claudia Pogoreutz Clinton A. Oakley Nils Rädecker Anny Cárdenas Gabriela Perna

Abstract Endozoicomonas are prevalent, abundant bacterial associates of marine animals, including corals. Their role in holobiont health and functioning, however, remains poorly understood. To identify potential interactions within the coral holobiont, we characterized the novel isolate Endozoicomonas marisrubri sp. nov. 6c and assessed its transcriptomic and proteomic response to tissue extracts of its native host, the Red Sea coral Acropora humilis. We show that coral tissue extracts stimulated differential expression of genes putatively involved in symbiosis establishment via the modulation of the host immune response by E. marisrubri 6c, such as genes for flagellar assembly, ankyrins, ephrins, and serpins. Proteome analyses revealed that E. marisrubri 6c upregulated vitamin B1 and B6 biosynthesis and glycolytic processes in response to holobiont cues. Our results suggest that the priming of Endozoicomonas for a symbiotic lifestyle involves the modulation of host immunity and the exchange of essential metabolites with other holobiont members. Consequently, Endozoicomonas may play an important role in holobiont nutrient cycling and may therefore contribute to coral health, acclimatization, and adaptation.

Holobiont

Anthozoa

Coral bleaching

Chordate

10.1038/s41396-022-01226-7

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Citations (71)

The potential for coral reef establishment through free-living stabilization

Scientific Reports (2017)

Sebastian Hennige Heidi L. Burdett Gabriela Perna Alexander W. Tudhope Nicholas A. Kamenos

Corals thrive in a variety of environments, from low wave and tidal energy lagoons, to high energy tidal reef flats, but remain dependent upon suitable substrate. Herein we reviewed the phenomenon of free-living corals (coralliths), examined whether they have the capacity to create their own stable habitat in otherwise uninhabitable, poor substrate environments through 'free-living stabilization', and explore their potential ecological role on coral reefs. This stabilization could be achieved by coral settlement and survival on mobile substrate, with subsequent growth into free-living coralliths until a critical mass is reached that prevents further movement. This allows for secondary reef colonization by other coral species. To preliminarily test this hypothesis we provide evidence that the potential to support secondary coral colonisation increases with corallith size. Due to the limited diversity of corallith species observed here and in the literature, and the lack of physiological differences exhibited by coralliths here to static controls, it seems likely that only a small selection of coral species have the ability to form coralliths, and the potential to create their own stable habitat.

Colonisation

Aquaculture of coral

10.1038/s41598-017-13668-7

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Flexibility in Red Sea Tridacna maxima‐Symbiodiniaceae associations supports environmental niche adaptation

Ecology and Evolution (2021)

Susann Rossbach Benjamin C. C. Hume Anny Cárdenas Gabriela Perna Christian R. Voolstra

Abstract Giant clams (Tridacninae) are important members of Indo‐Pacific coral reefs and among the few bivalve groups that live in symbiosis with unicellular algae (Symbiodiniaceae). Despite the importance of these endosymbiotic dinoflagellates for clam ecology, the diversity and specificity of these associations remain relatively poorly studied, especially in the Red Sea. Here, we used the internal transcribed spacer 2 (ITS2) rDNA gene region to investigate Symbiodiniaceae communities associated with Red Sea Tridacna maxima clams. We sampled five sites spanning 1,300 km (10° of latitude, from the Gulf of Aqaba, 29°N, to the Farasan Banks, 18°N) along the Red Sea's North‐South environmental gradient. We detected a diverse and structured assembly of host‐associated algae with communities demonstrating region and site‐specificity. Specimens from the Gulf of Aqaba harbored three genera of Symbiodiniaceae, Cladocopium, Durusdinium , and Symbiodinium , while at all other sites clams associated exclusively with algae from the Symbiodinium genus. Of these exclusively Symbiodinium ‐associating sites, the more northern (27° and 22°) and more southern sites (20° and 18°) formed two separate groupings despite site‐specific algal genotypes being resolved at each site. These groupings were congruent with the genetic break seen across multiple marine taxa in the Red Sea at approximately 19°, and along with our documented site‐specificity of algal communities, contrasted the panmictic distribution of the T. maxima host. As such, our findings indicate flexibility in T. maxima ‐Symbiodiniaceae associations that may explain its relatively high environmental plasticity and offers a mechanism for environmental niche adaptation.

Symbiodinium

Dinoflagellate

Red algae

10.1002/ece3.7299

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Skin microbiome of black-tip reef shark (Carcharhinus melanopterus)

Claudia Pogoreutz Mauvis Gore Gabriela Perna Catriona Millar Robert Nestler

Carcharhinus

Source

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Urbanization comprehensively impairs biological rhythms in coral holobionts

Global Change Biology (2022)

Yaeli Rosenberg Noa Simon‐Blecher Maya Lalzar Ruth Yam Aldo Shemesh

Coral reefs are in global decline due to climate change and anthropogenic influences (Hughes et al., Conservation Biology, 27: 261-269, 2013). Near coastal cities or other densely populated areas, coral reefs face a range of additional challenges. While considerable progress has been made in understanding coral responses to acute individual stressors (Dominoni et al., Nature Ecology & Evolution, 4: 502-511, 2020), the impacts of chronic exposure to varying combinations of sensory pollutants are largely unknown. To investigate the impacts of urban proximity on corals, we conducted a year-long in-natura study-incorporating sampling at diel, monthly, and seasonal time points-in which we compared corals from an urban area to corals from a proximal non-urban area. Here we reveal that despite appearing relatively healthy, natural biorhythms and environmental sensory systems were extensively disturbed in corals from the urban environment. Transcriptomic data indicated poor symbiont performance, disturbance to gametogenic cycles, and loss or shifted seasonality of vital biological processes. Altered seasonality patterns were also observed in the microbiomes of the urban coral population, signifying the impact of urbanization on the holobiont, rather than the coral host alone. These results should raise alarm regarding the largely unknown long-term impacts of sensory pollution on the resilience and survival of coral reefs close to coastal communities.

Coral bleaching

Environmental change

10.1111/gcb.16144

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Citations (21)

Animal Microbiome (2019)

Claudia Pogoreutz Mauvis Gore Gabriela Perna Catriona Millar Robert Nestler

Abstract Background Sharks are in severe global decline due to human exploitation. The additional concern of emerging diseases for this ancient group of fish, however, remains poorly understood. While wild-caught and captive sharks may be susceptible to bacterial and transmissible diseases, recent reports suggest that shark skin may harbor properties that prevent infection, such as a specialized ultrastructure or innate immune properties, possibly related to associated microbial assemblages. To assess whether bacterial community composition differs between visibly healthy and insulted (injured) shark skin, we compared bacterial assemblages of skin covering the gills and the back from 44 wild-caught black-tip reef sharks ( Carcharhinus melanopterus ) from the Amirante Islands (Seychelles) via 16S rRNA gene amplicon sequencing. Results Shark skin-associated bacterial communities were diverse (5971 bacterial taxa from 375 families) and dominated by three families of the phylum Proteobacteria typical of marine organisms and environments ( Rhodobacteraceae , Alteromonadaceae , Halomonadaceae ). Significant differences in bacterial community composition of skin were observed for sharks collected from different sites, but not between healthy or injured skin samples or skin type (gills vs. back). The core microbiome (defined as bacterial taxa present in ≥50% of all samples) consisted of 12 bacterial taxa, which are commonly observed in marine organisms, some of which may be associated with animal host health. Conclusion The conserved bacterial community composition of healthy and injured shark skin samples suggests absence of severe bacterial infections or substantial pathogen propagation upon skin insult. While a mild bacterial infection may have gone undetected, the overall conserved bacterial community implies that bacterial function(s) may be maintained in injured skin. At present, the contribution of bacteria, besides intrinsic animal host factors, to counter skin infection and support rapid wound healing in sharks are unknown. This represents clear knowledge gaps that should be addressed in future work, e.g. by screening for antimicrobial properties of skin-associated bacterial isolates.

10.1186/s42523-019-0011-5

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Citations (38)

Community-level sensitivity of a calcifying ecosystem to acute in situ CO2 enrichment

Marine Ecology Progress Series (2017)

Heidi L. Burdett Gabriela Perna Lucy McKay G Broomhead Nicholas A. Kamenos

MEPS Marine Ecology Progress Series Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections MEPS 587:73-80 (2018) - DOI: https://doi.org/10.3354/meps12421 Community-level sensitivity of a calcifying ecosystem to acute in situ CO2 enrichment Heidi L. Burdett1,2,*, Gabriela Perna3,4, Lucy McKay5,6, Gemma Broomhead5, Nicholas A. Kamenos4 1Lyell Centre for Earth and Marine Science and Technology, Edinburgh EH14 4AP, UK 2School of Energy, Geoscience, Infrastructure and Society, Heriot-Watt University, Edinburgh EH14 4AS, UK 3School of Geographical and Earth Science, University of Glasgow, Glasgow G12 8QQ, UK 4King Abdullah University for Science and Technology, Thuwal 23955, Saudi Arabia 5School of Earth & Environmental Sciences, University of St Andrews, St Andrews KY16 9AL, UK 6School of Civil and Environmental Engineering, University of Strathclyde, Glasgow G1 1XJ, UK *Corresponding author: h.burdett@hw.ac.uk ABSTRACT: The rate of change in ocean carbonate chemistry is a vital determinant in the magnitude of effects observed. Benthic marine ecosystems are facing an increasing risk of acute CO2 exposure that may be natural or anthropogenically derived (e.g. engineering and industrial activities). However, our understanding of how acute CO2 events impact marine life is restricted to individual organisms, with little understanding for how this manifests at the community level. Here, we investigated in situ the effect of acute CO2 enrichment on the coralline algal ecosystem—a globally ubiquitous, ecologically and economically important habitat, but one which is likely to be sensitive to CO2 enrichment due to its highly calcified reef-like structures engineered by coralline algae. Most notably, we observed a rapid community-level shift to favour net dissolution rather than net calcification. Smaller changes from net respiration to net photosynthesis were also observed. There was no effect on the net flux of DMS/DMSP (algal secondary metabolites), nor on the nutrients nitrate and phosphate. Following return to ambient CO2 levels, only a partial recovery was seen within the monitoring timeframe. This study highlights the sensitivity of biogenic carbonate marine communities to acute CO2 enrichment and raises concerns over the capacity for the system to 'bounce back' if subjected to repeated acute high-CO2 events. KEY WORDS: Calcification · Photosynthesis · Community · Ecosystem · Maerl bed · Carbon dioxide · Acidification Full text in pdf format Supplementary material PreviousNextCite this article as: Burdett HL, Perna G, McKay L, Broomhead G, Kamenos NA (2018) Community-level sensitivity of a calcifying ecosystem to acute in situ CO2 enrichment. Mar Ecol Prog Ser 587:73-80. https://doi.org/10.3354/meps12421 Export citation RSS - Facebook - Tweet - linkedIn Cited by Published in MEPS Vol. 587. Online publication date: January 25, 2018 Print ISSN: 0171-8630; Online ISSN: 1616-1599 Copyright © 2018 Inter-Research.

Ocean Acidification

Marine ecosystem

10.3354/meps12421

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Citations (15)

Data for "Heat stress reduces the contribution of diazotrophs to coral holobiont nitrogen cycling"

Zenodo (CERN European Organization for Nuclear Research) (2021)

Nils Rädecker Claudia Pogoreutz Hagen M. Gegner Anny Cárdenas Gabriela Perna

Raw data associated with publication 'Heat stress reduces the importance of diazotrophs for coral holobiont nitrogen cycling'. "Rädecker_etal_16S.csv" contains sequence abundance data of annotated 16S rRNA ASVs for all five coral colonies during control or heat stress conditions at day 10 of the experiment. "Rädecker_etal_nifH.csv" contains sequence abundance data of annotated nifH rRNA ASVs for all five coral colonies during control or heat stress conditions at day 10 of the experiment. "Rädecker_etal_N2Fix.csv" contains bulk (acetylene reduction) as well as net (15N2 assimilation) measurements of microbial nitrogen fixation for all five coral colonies during control or heat stress conditions at day 10 of the experiment. "Rädecker_etal_NanoSIMS.csvv" contains raw mass count data of coral host and algal symbiont ROIs (15 images per treatment) for one coral colony during control or heat stress conditions at day 10 of the experiment.

Holobiont

Cycling

Nitrogen Cycle

10.5281/zenodo.5552980

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Inherent differential microbial assemblages and functions associated with corals exhibiting different thermal phenotypes

Science Advances (2025)

Erika P. Santoro Anny Cárdenas Helena D. M. Villela Caren L. S. Vilela Angela Michelato Ghizelini

Certain coral individuals exhibit enhanced resistance to thermal bleaching, yet the specific microbial assemblages and their roles in these phenotypes remain unclear. We compared the microbial communities of thermal bleaching–resistant (TBR) and thermal bleaching–sensitive (TBS) corals using metabarcoding and metagenomics. Our multidomain approach revealed stable distinct microbial compositions between thermal phenotypes. Notably, TBR corals were inherently enriched with microbial eukaryotes, particularly Symbiodiniaceae, linked to photosynthesis, and the biosynthesis of antibiotic and antitumor compounds and glycosylphosphatidylinositol-anchor proteins, crucial for cell wall regulation and metabolite exchange. In contrast, TBS corals were dominated by bacterial metabolic genes related to nitrogen, amino acid, and lipid metabolism. The inherent microbiome differences between TBR and TBS corals, already observed before thermal stress, point to distinct holobiont phenotypes associated to thermal bleaching resistance, offering insights into mechanisms underlying coral response to climate-induced stress.

10.1126/sciadv.adq2583

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Corrigendum: Using Aiptasia as a Model to Study Metabolic Interactions in Cnidarian-Symbiodinium Symbioses

Frontiers in Physiology (2018)

Nils Rädecker Jean‐Baptiste Raina Mathieu Pernice Gabriela Perna Paul Guagliardo

Reason for Corrigendum:During submission of the final version of the manuscript for publication, a previous version of Figure 3 was accidentally uploaded. The labeling of this previous Figure version does not match the annotation in the figure legend. The correct version of Figure 3 and its legend appear below. The authors sincerely apologize for the error. This error does not change the scientific conclusions of the research article.

Symbiodinium

Legend

10.3389/fphys.2018.00449

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Citations (3)