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Microbiota of healthy and bleached corals of the species Siderastrea stellata in response to river influx and seasonality in Brazilian northeast

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Abstract

Although coral bleaching is increasing worldwide due to warming oceans exacerbated by climate change, there has been a growing recognition that local stressors may play an additional role. Important stressors include the physicochemical and microbiological influences that are related to river runoff. Here, we investigated the microbiota associated to mucus and tissue of endemic coral Siderastrea stellata, collected from Brazilian northeast coral reefs of Barra de Santo Antônio (subject to river runoff) and Maragogi (minimal river runoff) during both the rainy and dry seasons. We sequenced the V4 region of 16S rDNA and used multiple R packages to process raw data and performed statistical analysis to reveal the microbial community structure composition and functional predictions. Major dissimilarities between microbial communities were related to seasonality, while healthy and bleached specimens were mainly associated with the enrichment of several less abundant taxa involved in specific metabolic functions, mainly related to the nitrogen cycle. We were not able to observe the dominance of groups that has been previously associated with bleachings, such as Vibrionaceae or Burkholderiaceae. The influx of freshwater appears to increase the homogeneity between individuals in Barra de Santo Antonio, especially during the rainy season. By contrast, we observed an increased homogeneity between samples in Maragogi during the dry season. Understanding the dynamics of the coral microbiota and how bleaching appears in response to specific environmental variables, in addition to determining the conditions that lead to a more robust coral microbiota, is essential for choosing the most appropriate area and conservation methods, for example.

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Data availability

The DNA sequences generated during the current study are available in the GenBank repository.

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Acknowledgements

This work is part of the Long Term Ecological Research–Brazil coral reef PELD-CCAL (Projeto Ecológico de Longa Duração—Costa dos Corais, Alagoas) and was funded by the Brazilian National Council for Scientific and Technological Development CNPq – (CNPq, process numbers 408718/2013-7, 441657/2016-8, 311553/2018-4, 312889/2021-6), FAPEAL—Research Support Foundation of the State of Alagoas (#60030.1564/2016) and by Coordination for the Improvement of Higher Education Personnel CAPES-Brazil CAPES (#23038.000452/2017-16). The authors would like to thank the Genomics and Bioinformatics Center of Drug Research and Development Center of Federal University of Ceará, Brazil, for DNA sequencing.

Funding

This research was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, number of grants 408718/2013–7, 441657/2016–8, 311553/2018–4, and 312889/2021–6), FAPEAL—Research Support Foundation of the State of Alagoas (#60030.1564/2016), and by Coordination for the Improvement of Higher Education Personnel CAPES-Brazil CAPES (#23038.000452/2017–16).

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Authors and Affiliations

Authors

Contributions

Gustavo Vasconcelos Bastos Paulino: conceptualization, formal analysis, investigation, writing—original draft, and visualization. Ciro Ramon Félix: investigation, formal analysis, and writing—review and editing. Francisca Andréa da Silva Oliveira: resources and writing—review and editing. Cinta Gomez-Silvan: resources. Vânia M. M. Melo: resources and writing—review and editing. Gary L. Andersen: data curation, writing—review and editing, resources, and supervision. Melissa Fontes Landell: data curation, writing—review and editing, resources, supervision, and funding acquisition.

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Correspondence to Melissa Fontes Landell.

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Supplementary Information

ESM 1

Supplementary figure 1: Health status of the samples of coral Siderastrea stellata. (A) bleached, (B) moderately bleached, and (C) healthy.(PNG 7450 kb)

ESM 2

Supplementary figure 2: Rarefaction curve used to determine the minimum value of reads used in statistical analysis. According to the results, it was possible to demonstrate that the sampling depth used in the statistical samples was sufficient to adequately represent the bacterial communities.(PNG 185 kb)

ESM 3

Supplementary figure 3: Relative abundance of top-10 classes. Samples are grouped according to seasons (rainy and dry) and health conditions (healthy or bleached).(PNG 51 kb)

High resolution image (TIF 221 kb)

ESM 4

Supplementary figure 4: Relative abundance of top-10 families. Samples are grouped according to seasons (rainy and dry) and health conditions (healthy or bleached).(PNG 49 kb)

High resolution image (TIF 211 kb)

ESM 5

Supplementary figure 5: Relative abundance of functional groups related to nitrogen utilization predicted using FAPROTAX in A) Barra de Santo Antônio and B) Maragogi. In general, the relative abundance was reduced for functional categories related to the nitrogen cycle in bleached corals, with the exception of the nitrification category(PNG 34 kb)

High resolution image (TIF 94 kb)

ESM 6

Supplementary figure 6: Principal Coordinates Analysis (PCA) plot based on predicted metagenomic content of healthy and bleached samples of coral Siderastrea stellata collected during the rainy (April) and dry (September) seasons in two distinct coral reefs (Barra de Santo Antônio e Maragogi – Brazil).(PNG 38 kb)

High resolution image (TIF 116 kb)

ESM 7

Supplementary table 1: Values of physicochemical parameters measured during each collection. The results of PERMANOVA analysis suggested that the only parameter that significantly influenced differences between samples from the same reef at different seasons was precipitation (F = 1.8135, R2 = 0.21385 and p-value = 1e04).(DOCX 13 kb)

ESM 8

Supplementary table 2: Taxa that according to the DESeq2 algorithm showed statistically significant differential abundance between the two treatments, where (+) indicates enrichment in healthy corals and (-) in bleached corals. The results revealed that differences between healthy and bleached corals could be attributed mainly to “rare” microbiota members, which varied in response to seasonality(DOCX 24 kb)

ESM 9

Supplementary table 3: KEGG pathways mainly associated to each treatment after analysis with DESeq2 algorithm identify significant differentially abundant KO between healthy (+) and (-) bleached corals. The results indicated that there was significant variation for 58 KO groups, of which 46 KO groups (corresponding to 30 pathways) were enriched in healthy corals.

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Paulino, G.V.B., Félix, C.R., da Silva Oliveira, F.A. et al. Microbiota of healthy and bleached corals of the species Siderastrea stellata in response to river influx and seasonality in Brazilian northeast. Environ Sci Pollut Res 30, 26496–26509 (2023). https://doi.org/10.1007/s11356-022-23976-9

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