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Gut Microbiota in Decapod Shrimps: Evidence of Phylosymbiosis

  • Host Microbe Interactions
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A Correction to this article was published on 21 August 2021

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Abstract

Gut microbiota have long attracted the interest of scientists due to their profound impact on the well-being of animals. A non-random pattern of microbial assembly that results in a parallelism between host phylogeny and microbial similarity is described as phylosymbiosis. Phylosymbiosis has been consistently observed in different clades of animal hosts, but there have been no studies on crustaceans. In this study, we investigated whether host phylogeny has an impact on the gut microbiota assemblages in decapod shrimps. We examined the gut microbial communities in 20 shrimp species from three families inhabiting distinct environments, using metabarcoding analyses of the V1–V3 hypervariable region of the 16S rRNA gene. Gut microbial communities varied within each shrimp group but were generally dominated by Proteobacteria. A prevalent phylosymbiotic pattern in shrimps was evidenced for the first time by the observations of (1) the distinguishability of microbial communities among species within each group, (2) a significantly lower intraspecific than interspecific gut microbial beta diversity across shrimp groups, (3) topological congruence between host phylogenetic trees and gut microbiota dendrograms, and (4) a correlation between host genetic distances and microbial dissimilarities. Consistent signals of phylosymbiosis were observed across all groups in dendrograms based on the unweighted UniFrac distances at 99% operational taxonomic units (OTUs) level and in Mantel tests based on the weighted UniFrac distances based on 97% OTUs and amplicon sequence variants. Penaeids exhibited phylosymbiosis in most tests, while phylosymbiotic signals in atyids and pandalids were only detected in fewer than half of the tests. A weak phylogenetic signal was detected in the predicted functions of the penaeid gut microbiota. However, the functional diversities of the two caridean groups were not significantly related to host phylogeny. Our observations of a parallelism in the taxonomy of the gut microbiota with host phylogeny for all shrimp groups examined and in the predicted functions for the penaeid shrimps indicate a tight host-microbial relationship during evolution.

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Data Availability

Sequences used for host phylogeny construction were deposited in the NCBI Nucleotide database with accession numbers MT540493-MT540497 (for atyid 16S rRNA), MT553844-MT553853 (for atyid NaK and enolase), and MT540544-MT540551 (for pandalid 16S rRNA). Raw reads of metabarcoding sequencing are available in the NCBI Sequence Read Archive under the Bioproject accession PRJNA635372.

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Acknowledgements

We thank T.Y. Chan, National Taiwan Ocean University, for his support to our field trip in collecting the pandalid samples; L.M. Tsang, The Chinese University of Hong Kong, for providing information on sample collection; and T.T. Tsang, The Chinese University of Hong Kong, for assistance in PICRUSt2 analyses. David Wilmshurst edited the final version of the manuscript.

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Funding

This work was supported by grants from the Collaborative Research Fund (project no. C4042-14G) of the Research Grants Council, Hong Kong SAR Government and the Hong Kong Branch of Southern Marine Science and Technology Guangdong Laboratory (Guangzhou), China.

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Authors and Affiliations

  1. Simon F.S. Li Marine Science Laboratory, School of Life Sciences, The Chinese University of Hong Kong, Hong Kong, SAR, China

    Yuanyuan Tang, Ka Yan Ma, Yaqin Wang, Xuelei Hu & Ka Hou Chu

  2. School of Ecology, Sun Yat-sen University, Guangzhou, China

    Ka Yan Ma

  3. Department of Surgery, The Chinese University of Hong Kong, Hong Kong, SAR, China

    Man Kit Cheung

  4. Institute of Marine Biology, National Taiwan Ocean University, Keelung, Taiwan

    Chien-Hui Yang

  5. School of Biology and Food Engineering, Guangdong University of Education, Guangzhou, China

    Xuelei Hu

  6. Food Research Centre, School of Life Sciences, The Chinese University of Hong Kong, Hong Kong, SAR, China

    Hoi Shan Kwan

  7. Hong Kong Branch of Southern Marine Science and Technology Guangdong Laboratory (Guangzhou), Hong Kong, SAR, China

    Ka Hou Chu

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Contributions

K.H. Chu, Y. Tang, and K.Y. Ma designed and conceived the idea. Y. Tang conducted the experiments, analyzed the data, and wrote the manuscript. M.K. Cheung provided suggestions for data analyses. C.-H. Yang provided the 16S rRNA gene sequences of pandalids. X. Hu and Y. Wang assisted sample collection. K.Y. Ma, M.K. Cheung, H.S. Kwan, and K.H. Chu revised the manuscript. K.H. Chu supervised and monitored the project.

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Correspondence to Ka Hou Chu.

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Supplementary Information

ESM 1

ESM 2

ST1 Breakdown of high-quality reads by species.

ESM 3

ST2 Importance scores of features at the bacterial genus level.

ESM 4

ST3 Descriptions of the top 10 abundant predicted functional pathways.

ESM 5

SF1 Host phylogenetic trees with outgroups.

ESM 6

SF2 Diversity and PICRUSt2 results based on 97% OTUs and ASVs.

ESM 7

SF3 Microbiota dendrograms constructed using 97% OTUs and ASVs.

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Tang, Y., Ma, K.Y., Cheung, M.K. et al. Gut Microbiota in Decapod Shrimps: Evidence of Phylosymbiosis. Microb Ecol 82, 994–1007 (2021). https://doi.org/10.1007/s00248-021-01720-z

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