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Deciphering pH-dependent microbial taxa and functional gene co-occurrence in the coral Galaxea fascicularis

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Abstract

How the coral microbiome responds to oceanic pH changes due to anthropogenic climate change, including ocean acidification and deliberate artificial alkalization, remains an open question. Here, we applied a 16S profile and GeoChip approach to microbial taxonomic and gene functional landscapes in the coral Galaxea fascicularis under three pH levels (7.85, 8.15, and 8.45) and tested the influence of pH changes on the cell growth of several coral-associated strains and bacterial populations. Statistical analysis of GeoChip-based data suggested that both ocean acidification and alkalization destabilized functional cores related to aromatic degradation, carbon degradation, carbon fixation, stress response, and antibiotic biosynthesis in the microbiome, which are related to holobiont carbon cycling and health. The taxonomic analysis revealed that bacterial species richness was not significantly different among the three pH treatments, but the community compositions were significantly distinct. Acute seawater alkalization leads to an increase in pathogens as well as a stronger taxonomic shift than acidification, which is worth considering when using artificial ocean alkalization to protect coral ecosystems from ocean acidification. In addition, our co-occurrence network analysis reflected microbial community and functional shifts in response to pH change cues, which will further help to understand the functional ecological role of the microbiome in coral resilience.

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Data Availability

GeoChip metadata have been deposited in the Gene Expression Omnibus (GEO) database under accession codes GSE182928 and GPL30559. Raw 16S high-throughput sequencing data have been deposited in the NCBI database under accession number PRJNA594758. The 16S rDNA sequences of all representative isolates in this study have been deposited in GenBank under accession numbers MZ950544-MZ950604.

Funding

This research was financially supported by the Natural Science Foundation of China (NSFC-41906094), the Fujian Provincial Science and Technology Project (Grants 2020N5011) and the Fujian Provincial Natural Resources Science and Technology Innovation Project (Grants KY-090000-04-2022-006).

Author information

Authors and Affiliations

  1. Fujian Provincial Key Laboratory on Conservation and Sustainable Utilization of Marine Biodiversity, Fuzhou Institute of Oceanography, Minjiang University, Fuzhou, 350108, China

    Zhenyue Lin & Jianming Chen

  2. Technology Innovation Center for Monitoring and Restoration Engineering of Ecological Fragile Zone in Southeast China, Ministry of Natural Resources, Fuzhou, 350001, China

    Zhenyue Lin & Jianming Chen

  3. Key Laboratory of Marine Ecological Conservation and Restoration, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, 361005, China

    Xinqing Zheng

  4. Observation and Research Station of Coastal Wetland Ecosystem in Beibu Gulf, Ministry of Natural Resources, Beihai, 356015, China

    Xinqing Zheng

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  1. Zhenyue Lin
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Contributions

Zhenyue Lin and Jianming Chen conceived and designed the study. Zhenyue Lin and Xinqing Zheng contributed to designing and optimizing the pH-stat CO2/N2 dosing systems. Zhenyue Lin wrote the manuscript.

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Correspondence to Zhenyue Lin or Jianming Chen.

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Supplementary information

Supplementary material 1

Table S1. Significance tests of the functional gene structure of the microbial communities among the three pH treatment groups. Three different permutation tests were performed, i.e., an MRPP, an ANOSIM, and an ADONIS, based on the Bray–Curtis or Jaccard distance. Table S2. Shannon, Pielou and Simpson indices representing α diversity for the 16S- profiles; there were no significant differences among the three pH treatment groups (p>0.05, Kruskal–Wallis test). Table S3. Number of isolates and taxonomy listings obtained from the multiple carbon source culture media employed. Table S4. Information on 74 isolates that were recovered from the coral G. fascicularis. Table S5. Effects of different media pH values on the doubling time of the selected representative bacterial isolates. Table S6. Effects of different media and pH values on the doubling time of culturable bacterial population growth.

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Lin, Z., Zheng, X. & Chen, J. Deciphering pH-dependent microbial taxa and functional gene co-occurrence in the coral Galaxea fascicularis. Microb Ecol 86, 1856–1868 (2023). https://doi.org/10.1007/s00248-023-02183-0

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