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Ectohydrolytic enzyme activities of bacteria associated with Orbicella annularis coral

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Abstract

Ectohydrolytic enzyme activity (EEA) potential of 37 bacterial isolates derived from Orbicella annularis coral and 2 coral pathogens (Vibrio shilonii and V. coralliilyticus) was measured as model to infer the role of bacteria in organic matter processing within coral reef ecosystems. Bacterial cell-specific activities of eight enzyme types were measured after incubation in organic matter enriched and unenriched filtered seawater. Max value of activities of alkaline phosphatase, oleate-lipase, stearate-lipase and proteinase were 769.3, 327.6, 82.9 and 36.7 amol cell−1 h−1, respectively. Chitinase, α-mannosidase, α-glucosidase and β-glucosidase were generally lower by comparison (max 4.7–20.7 amol cell−1 h−1). No “super” isolates (bacteria expressing high levels of all ectohydrolases) were found suggesting a “specialization” among individual bacterial strains. Cumulatively, the 39 isolates tested displayed a broad range of cell-specific enzyme activities in both organic matter conditions. Culture-independent measurement of coral mucus layer EEA in O. annularis off a Panama reef showed comparable EEA patterns and diversity as the isolates. Volume-specific EEAs of all enzymes except alkaline phosphatase were 8–48 times higher in mucus than in surrounding seawater (SSW) samples. However, cell-specific EEAs in mucus were generally lower than in the SSW partly due to more abundant cells in the mucus than in SSW. For field samples, ≥ 85% of proteinase was cell-bound, while lipase was preferentially dissolved (40–96%). In general, the production of dissolved EEAs varied among measurements depending on sample source and enzyme types, suggesting a potential role of ectoenzyme size distribution in linking the whole reef ecosystem. Our findings support that the cumulative ectoenzyme expression (“ectoenzymome”) of the coral microbiome has the potential to maintain the functional resilience of the coral holobiont and response to stress through its contribution to organic matter processing within coral reef ecosystems.

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Acknowledgements

This research was supported by grant #4827 from Gordon and Betty Moore Foundation to FA, Project 42076150 supported by National Natural Science Foundation of China (NSFC) to XM, Project 41877352 (NSFC), Shenzhen Fundamental Research and Discipline Layout project (JCYJ20180507182227257) and the Guangdong MEPP fund (GDOE[2019]A06) to XZ, China Scholarship Council (CSC) and #LMB20191102 from South China Sea Institute of Oceanology Chinese Academy of Sciences to YZ and NSF OCE (1442206) to MM. Lastly, we would like to thank our editor and the reviewers for their great advice.

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Authors and Affiliations

  1. Shenzhen International Graduate School, Tsinghua University, Shenzhen, 518055, China

    Yanyan Zhou, Xian-zhong Mao & Xiaoshan Zhu

  2. Marine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, CA, La Jolla, USA

    Yanyan Zhou, Ryan Guillemette, Francesca Malfatti & Farooq Azam

  3. State Key Laboratory of Marine Environmental Science and Key Laboratory of the MOE for Coastal and Wetland Ecosystems, School of Life Sciences, Xiamen University, Xiamen, China

    Yanyan Zhou & Tianling Zheng

  4. Pacific Coastal Ecology Branch, U.S. Environmental Protection Agency, Newport, OR, 97365, USA

    Ryan Guillemette

  5. University of Trieste, Trieste, Italy

    Francesca Malfatti

  6. Department of Biology, Pennsylvania State University, University Park, PA, USA

    Mónica Medina

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Zhou, Y., Guillemette, R., Malfatti, F. et al. Ectohydrolytic enzyme activities of bacteria associated with Orbicella annularis coral. Coral Reefs 40, 1899–1913 (2021). https://doi.org/10.1007/s00338-021-02188-6

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