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Core gut microbial communities are maintained by beneficial interactions and strain variability in fish

Nature Microbiology volume 4, pages 2456–2465 (2019)Cite this article

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Abstract

The term core microbiome describes microbes that are consistently present in a particular habitat. If the conditions in that habitat are highly variable, core microbes may also be considered to be ecological generalists. However, little is known about whether metabolic competition and microbial interactions influence the ability of some microbes to persist in the core microbiome while others cannot. We investigated microbial communities at three sites in the guts of European seabass under four dietary conditions. We identified generalist core microbial populations in each gut site that are shared across fish, present under multiple diets and persistent over time. We found that core microbes tend to show synergistic growth in co-culture, and low levels of predicted and validated metabolic competition. Within core microbial species, we found high levels of intraspecific variability and strain-specific habitat specialization. Thus, both intraspecific variability and interspecific facilitation may contribute to the ecological stability of the animal core microbiome.

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Fig. 1: Habitat filtering by gut part shapes seabass gut microbial communities.
Fig. 2: A core microbial community composed of 8 abundant generalist species persists across different habitats of diets and gut parts, and across different species of fish.
Fig. 3: Facilitation and positive interactions are prevalent among identified generalist core microbes.
Fig. 4: Generalist core species show higher strain variability, which is congruent with their habitat preferences.

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Data availability

Sequencing data are provided at the NCBI (SRA) database under the study accession code SRP118834. The non-sequencing related data are provided in Supplementary Data 1.

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Acknowledgements

The research described here was supported by grants from the European Research Council under the European Union’s Horizon 2020 research and innovation program (grant no. 640384), the Israel Science Foundation (grant no. 1947/19) and the Chief Scientist of the Ministry of Agriculture and Rural Development (grant no. 356-0665-14).

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Authors and Affiliations

  1. Department of Life Sciences, Ben-Gurion University of the Negev and the National Institute for Biotechnology in the Negev, Marcus Family Campus, Be’er-Sheva, Israel

    Fotini Kokou, Goor Sasson, Stav Eyal, Ofer Ovadia & Itzhak Mizrahi

  2. Department of Poultry and Aquaculture, Institute of Animal Sciences, Agricultural Research Organization, Rishon LeZion, Israel

    Fotini Kokou, Sheenan Harpaz & Avner Cnaani

  3. Institute of Plant Sciences and Genetics in Agriculture, Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel

    Jonathan Friedman

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Contributions

F.K. conducted the experiments, molecular work and sequencing, analysed and interpreted the sequencing and molecular data, and wrote the manuscript. G.S. analysed some of the sequencing data. J.F. analysed some of the sequencing data and provided advice on analysis. S.E. conducted some of the microbiology experiments and isolation. O.O. consulted on the interpretation of the data. S.H. and A.C. helped with animal experiments and with the supervision and financial support of the project. I.M. obtained the funding, supervised the study, analysed and interpreted the data, financially managed the project and wrote the manuscript.

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Correspondence to Itzhak Mizrahi.

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Supplementary information

Supplementary Information

Supplementary Tables 1–19, Supplementary Figs. 1–14 and Supplementary References.

Reporting Summary

Supplementary Data for Supplementary Table 16

Median richness of strains per part is presented in the table along with the P values after comparison of the strain richness between the different gut parts (n = 36 fish per part). Empty cells indicate non-significant P values for the one-sided tests performed (as it is indicated below the Wilcoxon P values in the table). The average occurrence and median abundance is also calculated in the table for the different parts, showing no significant differences in the abundances of these OTUs. The right two columns show the average abundance of strains that show niche expansion patterns compared with the strains that do not show the patterns.

Supplementary Data for Supplementary Table 17

Clusters with 97% sequence similarity of microbes, showing major and minor sequences per OTU, as described in the ‘Quantification of sequencing noise’ section in the Methods.

Supplementary Data 1

Quantitative PCR from microbial interactions using specific primers. The growth results are expressed in copy number μl−1 (using specific primers for each microbe) and the experiment was performed in triplicate.

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Kokou, F., Sasson, G., Friedman, J. et al. Core gut microbial communities are maintained by beneficial interactions and strain variability in fish. Nat Microbiol 4, 2456–2465 (2019). https://doi.org/10.1038/s41564-019-0560-0

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