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Archaeal communities of low and high microbial abundance sponges inhabiting the remote western Indian Ocean island of Mayotte

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Abstract

Marine sponges are abundant and ecologically important components of coral reefs and have been shown to harbour exceptionally high microbial densities, which can differ substantially among sponge species. However, this dichotomy between high and low microbial abundance (HMA, LMA) sponges is still not fully understood, particularly as concerns the archaeal community. This study aims to fill this gap by analysing (using 454-pyrosequencing of the 16S rRNA gene) how the archaeal community varies among known LMA (Stylissa carteri, and Stylissa massa), known HMA (Hyrtios erectus and Xestospongia testudinaria) and unknown HMA/LMA status sponge species (Ectyoplasia coccinea, Paratetilla bacca and Petrosia aff. spheroida) collected in a remote location in which very few sponge microbial composition studies have been previously performed (Mayotte, Comores archipelago, France) and comparing the results with those reported in four other geographical areas. Based on archaeal community composition, the known LMA sponges formed a distinct cluster together with Paratetilla bacca, Ectyoplasia coccinea and seawater while the known HMA sponge X. testudinaria formed a cluster with Petrosia aff. spheroida. The known HMA sponge H. erectus, in turn, had an intermediate archaeal community between HMA sponges and sediment samples. In addition to the above, we also showed significant compositional congruence between archaeal and bacterial communities sampled from the same sponge individuals. HMA sponges were mainly dominated by members assigned to the genus Nitrosopumilus while LMA sponges were mainly dominated by members assigned to the genus Cenarchaeum. In general, there was no clear difference in richness between HMA and LMA sponges. Evenness, however, was higher in HMA than LMA sponges. Whilst the present study corroborates some of the traits commonly associated with the HMA–LMA dichotomy (higher evenness in Mayotte HMA sponges), this was not consistent across geographical areas showing that more research is needed to fully understand the HMA/LMA dichotomy as concerns Archaea.

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Availability of data and materials

The DNA sequences generated in this study can be downloaded from the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA): SRP071901: PRJNA315454.

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Acknowledgements

Research permits were issued via the Prefecture of Mayotte. We thank Cécile Debitus, Bruno Fichou, Stephan Aubert, Philippe Prost, and Jean‐Pierre Bellanger for their support.

Funding

This study was financed through the ANR‐Netbiome under grant No ANR‐11‐EBIM‐0006 and a contribution to the project LESS CORAL [PTDC/AAC-AMB/115304/2009] funded by FEDER, through COMPETE2020 - Programa Operacional Competitividade e Internacionalização (POCI), and by national funds (OE), through the Portuguese Foundation for Science and Technology (FCT)/MCTES. Thanks are also due, to FCT/MCTES for the financial support to CESAM (UIDP/50017/2020 + UIDB/50017/2020), through national funds. Ana R.M. Polónia was supported by a postdoctoral scholarship (SFRH/BPD/117563/2016) funded by FCT/MCTES and by the European Social Fund (ESF).

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Authors and Affiliations

  1. LEMAM - Laboratory for Molecular Studies of Marine Environments, CESAM - Centre for Environmental and Marine Studies, Department of Biology, University of Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal

    Ana Rita Moura Polónia & Daniel Francis Richard Cleary

  2. CHEMBIOPRO (Laboratoire de Chimie et de Biotechnologie des Produits Naturels), Saint-Denis, France

    Anne Gauvin‐Bialecki

  3. Naturalis Biodiversity Center, Leiden, The Netherlands

    Nicole Joy de Voogd

  4. Institute of Environmental Sciences, Leiden University, Leiden, The Netherlands

    Nicole Joy de Voogd

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  1. Ana Rita Moura Polónia
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  2. Daniel Francis Richard Cleary
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  3. Anne Gauvin‐Bialecki
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  4. Nicole Joy de Voogd
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Contributions

N.J.d.V. and D.F.R.C. designed the study; N.J.d.V. and A.G.B. collected the samples; A.R.M.P. performed the laboratory work; D.F.R.C. and A.R.M.P. performed the data analysis; A.R.M.P., D.F.R.C., A.G.B., and N.J.d.V wrote the manuscript.

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Correspondence to Ana Rita Moura Polónia.

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Supplementary information

Below is the link to the supplementary information.

Supplementary Fig. 1

(a) Location map with (b) inset showing the island of Mayotte (PDF 182 kb)

Supplementary Fig. 2

Relative abundance of the most abundant classes in the demosponges Paratetilla bacca (Pb), Stylissa carteri (Sc), Stylissa massa (Sm), Ectyoplasia coccinea (Ec), Hyrtios erectus (He), Petrosia aff. spheroida (Ps), Xestospongia testudinaria (Xt); sediment (Sd), and seawater (Wt) (PDF 35 kb)

Supplementary Table 1

Sample list with the sample code, sponge species, Group code, Host, high microbial abundance (HMA) or low microbial abundance (LMA) type, collection site (location), and GPS coordinates (XLS 26 kb)

Supplementary Table 2

Results of emmeans analysis showing pairwise comparisons of differences in the relative abundances of selected phyla between biotopes based on the Tukey test. Significance: * 0.01 < Pr < 0.05 ** 0.001 < Pr < 0.01; *** Pr < 0.001 (XLS 52 kb)

Supplementary Table 3

Sample list with the sample code, biotope, number of replicates, total number of OTUs, number of core OTUs mean abundance of core OTUs, mean abundance of the single most abundant OTUs, number of specific OTUs, Diversity, Richness and Evenness. (XLS 36 kb)

Supplementary Table 4

Results of simper analysis showing the contribution of OTUs to differences in similarity between pairs of samples. OTUs that contribute significantly to differences are indicated: * 0.01 < P < 0.05 ** 0.001 < P < 0.01; *** P < 0.001 (XLSX 72 kb)

Supplementary Table 5

List of abundant (≥ 130 sequence reads) OTUs and closely related organisms identified using BLAST search. OTU: OTU number; Abund: number of sequence reads; Taxonomic classification, Acc: Genbank accession numbers of closely related organisms identified using BLAST; Seq: sequence similarity of these organisms with our representative OTU sequences; Source: isolation source of organisms identified using BLAST (XLS 36 kb)

Supplementary Table 6

List of abundant Mayotte OTUs with the same closely related organisms identified using BLAST search in other geographic areas. OTU: OTU number; Study: Geographic area; Reference: reference of the study in which the OTU were previous reported; Core: biotopes where the OTUs were core OTUs; Group: biotope where the OTUs were found; Abund: number of sequence reads; Database: Database used in QIIME; Taxonomic classification; GI:GenBank GenInfo sequence identifiers; Acc: Genbank accession numbers of closely related organisms identified using BLAST; Seq: sequence similarity of these organisms with our representative OTU sequences; Source: isolation source of organisms identified using BLAST; Location: Geographic region of the organisms identified using BLAST. In the ‘Group’ category, the most dominant OTUs and the OTUs predominantly found in a given biotope (not considering OTUs ≤ 5 sequences) are indicated by one asterisk (*) and/or marked bold respectively. Sm: S. massa; Sc: S. carteri; Wt: Water; He: H. erectus; Ps: Petrosia aff. spheroida; Sed: Sediment; Xt: X. testudinaria; Ap: Aaptos lobata; Bie: Biemna fortis. (XLS 41 kb)

Supplementary Table 7

Mean and standard deviation (SD) of Diversity (H′), Richness (S) and Evenness (J) indices reported in the LMA sponge species S. massa and S. carteri and the HMA sponge species X. testudinaria and H. erectus (N: number of replicates) across several geographic regions. Makassar: Spermonde Archipelago coral reef system; Jakarta: Kepulauan Seribu Reef System, Berau: Berau reef system and Papua: Misool coral reef system, Indonesia resorting to the results published in our previous studies (Polónia et al. 2014; 2015; 2016; 2017; 2018). (XLS 42 kb)

Supplementary Table 8

Mean and standard deviation (SD) relative abundance of the Thaumarchaeota and Euryarchaeota phyla reported in the LMA sponge species S. massa and S. carteri and the HMA sponge species X. testudinaria and H. erectus (N: number of replicates) across several geographic regions. Makassar: Spermonde Archipelago coral reef system; Jakarta: Kepulauan Seribu Reef System, Berau: Berau reef system and Papua: Misool coral reef system, Indonesia resorting to the results published in our previous studies (Polónia et al. 2014; 2015; 2016; 2017; 2018). (XLS 41 kb)

Supplementary Table 9

Number of core OTUs (C.OTUs) the mean abundance of these core OTUs (C.OTUs(%)) and the mean abundance of the single most abundant OTU (D.OTU(%)) in the LMA sponge species S. massa and S. carteri and the HMA sponge species X. testudinaria and H. erectus (N: number of replicates) across several geographic regions. Makassar: Spermonde Archipelago coral reef system; Jakarta: Kepulauan Seribu Reef System, Berau: Berau reef system and Papua: Misool coral reef system, Indonesia resorting to the results published in our previous studies (Polónia et al. 2014; 2015; 2016; 2017; 2018). (XLS 39 kb)

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Polónia, A.R.M., Cleary, D.F.R., Gauvin‐Bialecki, A. et al. Archaeal communities of low and high microbial abundance sponges inhabiting the remote western Indian Ocean island of Mayotte. Antonie van Leeuwenhoek 114, 95–112 (2021). https://doi.org/10.1007/s10482-020-01503-5

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