Thank you for biting: dispersal of beneficial microbiota through 'antagonistic' interactions

Grupstra, Carsten G. B.; Lemoine, Nathan P.; Cook, Chelsea N.; Correa, Adrienne M. S.

doi:10.1016/j.tim.2022.03.006

Cited by 15 publications

(24 citation statements)

References 77 publications

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“…The authors noted that egesta released by H. crispa were consumed by symbiotic anemonefish ( Alan Verde, Cleveland & Lee, 2015 ). It is not known if other animals consume Aiptasia egesta in nature, but if so, they may aid in algal dispersal, as algae often survive digestion ( Parker, 1984 ; Grupstra et al, 2021 ; Grupstra et al, 2022 ).…”

Section: Discussionmentioning

confidence: 99%

Algae from Aiptasia egesta are robust representations of Symbiodiniaceae in the free-living state

Maruyama

Unsworth

Sawiccy

et al. 2022

PeerJ

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Many cnidarians rely on their dinoflagellate partners from the family Symbiodiniaceae for their ecological success. Symbiotic species of Symbiodiniaceae have two distinct life stages: inside the host, in hospite, and outside the host, ex hospite. Several aspects of cnidarian-algal symbiosis can be understood by comparing these two life stages. Most commonly, algae in culture are used in comparative studies to represent the ex hospite life stage, however, nutrition becomes a confounding variable for this comparison because algal culture media is nutrient rich, while algae in hospite are sampled from hosts maintained in oligotrophic seawater. In contrast to cultured algae, expelled algae may be a more robust representation of the ex hospite state, as the host and expelled algae are in the same seawater environment, removing differences in culture media as a confounding variable. Here, we studied the physiology of algae released from the sea anemone Exaiptasia diaphana (commonly called Aiptasia), a model system for the study of coral-algal symbiosis. In Aiptasia, algae are released in distinct pellets, referred to as egesta, and we explored its potential as an experimental system to represent Symbiodiniaceae in the ex hospite state. Observation under confocal and differential interference contrast microscopy revealed that egesta contained discharged nematocysts, host tissue, and were populated by a diversity of microbes, including protists and cyanobacteria. Further experiments revealed that egesta were released at night. In addition, algae in egesta had a higher mitotic index than algae in hospite, were photosynthetically viable for at least 48 hrs after expulsion, and could competently establish symbiosis with aposymbiotic Aiptasia. We then studied the gene expression of nutrient-related genes and studied their expression using qPCR. From the genes tested, we found that algae from egesta closely mirrored gene expression profiles of algae in hospite and were dissimilar to those of cultured algae, suggesting that algae from egesta are in a nutritional environment that is similar to their in hospite counterparts. Altogether, evidence is provided that algae from Aiptasia egesta are a robust representation of Symbiodiniaceae in the ex hospite state and their use in experiments can improve our understanding of cnidarian-algal symbiosis.

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Section: Discussionmentioning

confidence: 99%

Algae from Aiptasia egesta are robust representations of Symbiodiniaceae in the free-living state

Maruyama

Unsworth

Sawiccy

et al. 2022

PeerJ

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“…Our research, as well as two previous studies ( 11, 21 ), add an additional dimension to this relationship: herbivores can also disperse pathogens in their feces that cause lesions in coral tissues. More work is needed to test the extent to which different (herbivorous) fish species contribute to the dispersal of viable coral pathogens ( 5 ).…”

Section: Discussionmentioning

confidence: 99%

“…Consumers in diverse ecosystems fulfill important roles regarding the dispersal of microbiota ( 3, 5, 75, 76 ). Through the dispersal of microbiota, consumer activities affect the assembly of microbiota in resource species ( 5 ).…”

Section: Discussionmentioning

confidence: 99%

Consumer feces impact coral health in guild-specific ways

Grupstra

Howe‐Kerr

Meulen

et al. 2022

Preprint

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Microbiota from consumer feces can impact resource species in guild-specific ways. We tested the effect of fresh and heat-killed feces from corallivorous (coral-eating) and grazer/detritivorous fish on coral health and found that fresh grazer/detritivore feces, but not fresh corallivore feces, affected coral health in detrimental ways compared to heat-killed feces, suggesting that microbiota in grazer/detritivore feces were harmful. Bacterial diversity across 10 fish species suggests our experimental findings are generalizable to consumer guild: corallivore feces contained more coral-associated bacteria, and lower abundances of the coral pathogen, Vibrio coralliilyticus. These findings recontextualize the ecological roles of consumers on coral reefs: although herbivores support coral dominance through removal of algal competitors, they also disperse coral pathogens. Corallivore predation can wound corals, yet their feces contain potentially beneficial coral- associated bacteria, supporting the hypothesized role of corallivores in coral symbiont dispersal. Such consumer-mediated microbial dispersal as demonstrated here has broad implications for environmental management.

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“…Regional macroscale Symbiodiniaceae community structure (i.e., beta diversity) may also reflect chronic disturbance from anthropogenic activity (Claar et al, 2020a) and help identify more resilient or resistant reefs (Ziegler et al, 2015). Additionally, macroscale communities in reef seawater, sediments, feces, and on macro-algal surfaces may be important sources of symbiotic Symbiodiniaceae that can be acquired horizontally by prospective hosts (Adams et al, 2009;Ali et al, 2019;Castro-Sanguino and Sánchez, 2012;Coffroth et al, 2006;Cumbo et al, 2013;Fujise et al, 2021;Granados-Cifuentes et al, 2015;Grupstra et al, 2022bGrupstra et al, , 2021Nitschke et al, 2016;Porto et al, 2008;Quigley et al, 2018Quigley et al, , 2017aUmeki et al, 2020;Venera-Ponton et al, 2010). Symbiodiniaceae in a free-living mode may influence important processes, such as sexual reproduction, hybridization, and gene flow within Symbiodiniaceae (Figueroa et al, 2021).…”

Section: Why Study Symbiodiniaceae Community Diversity?mentioning

confidence: 99%

Building Consensus around the Assessment and Interpretation of Symbiodiniaceae Diversity

Davies¹,

Gamache²,

Howe‐Kerr³

et al. 2022

Preprint

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Within microeukaryotes, genetic and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellies), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.

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Thank you for biting: dispersal of beneficial microbiota through 'antagonistic' interactions

Cited by 15 publications

References 77 publications

Algae from Aiptasia egesta are robust representations of Symbiodiniaceae in the free-living state

Algae from Aiptasia egesta are robust representations of Symbiodiniaceae in the free-living state

Consumer feces impact coral health in guild-specific ways

Building Consensus around the Assessment and Interpretation of Symbiodiniaceae Diversity

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