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Prokaryote Communities Inhabiting Endemic and Newly Discovered Sponges and Octocorals from the Red Sea

  • Environmental Microbiology
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Abstract

In the present study, we assessed prokaryotic communities of demosponges, a calcareous sponge, octocorals, sediment and seawater in coral reef habitat of the central Red Sea, including endemic species and species new to science. Goals of the study were to compare the prokaryotic communities of demosponges with the calcareous sponge and octocorals and to assign preliminary high microbial abundance (HMA) or low microbial abundance (LMA) status to the sponge species based on compositional trait data. Based on the compositional data, we were able to assign preliminary LMA or HMA status to all sponge species. Certain species, however, had traits of both LMA and HMA species. For example, the sponge Ectyoplasia coccinea, which appeared to be a LMA species, had traits, including a relatively high abundance of Chloroflexi members, that were more typical of HMA species. This included dominant OTUs assigned to two different classes within the Chloroflexi. The calcareous sponge clustered together with seawater, the known LMA sponge Stylissa carteri and other presumable LMA species. The two dominant OTUs of this species were assigned to the Deltaproteobacteria and had no close relatives in the GenBank database. The octocoral species in the present study had prokaryotic communities that were distinct from sediment, seawater and all sponge species. These were characterised by OTUs assigned to the orders Rhodospirillales, Cellvibrionales, Spirochaetales and the genus Endozoicomonas, which were rare or absent in samples from other biotopes.

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Acknowledgements

We would like to thank Michael Campbell for providing the map. We are grateful for support in the field from the King Abdullah University of Science and Technology, including support from the Coastal and Marine Resources Core Lab.

Funding

This work is a contribution to the LESS CORAL project [PTDC/AAC-AMB/115304/2009] funded by FCT – Fundação para a Ciência e a Tecnologia , I.P., through national funds, and co-funding by FEDER, within the PT2020 Partnership Agreement and Compete 2020. Thanks are also due, for financial support to CESAM (UID/AMB/50017/2019), to FCT/MEC through national funds, and co-funding by the FEDER. Michael L. Berumen was supported by funding from KAUST (award no. CRG-1-814 2012-BER-002) and baseline research funds. Ana R.M. Polónia was supported by a postdoctoral scholarship (SFRH/BPD/117563/2016) funded by FCT, Portugal and national funds MCTES.

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Authors and Affiliations

  1. Department of Biology & CESAM, University of Aveiro, Campus de Santiago, 3810-193, Aveiro, Portugal

    D. F. R Cleary & A.R.M. Polónia

  2. Marine Biodiversity, Naturalis Biodiversity Center, Leiden, The Netherlands

    B.T. Reijnen & N. J. de Voogd

  3. Red Sea Research Center, Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal, 23955, Saudi Arabia

    M. L. Berumen

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

    N. J. de Voogd

Authors
  1. D. F. R Cleary
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  2. A.R.M. Polónia
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  3. B.T. Reijnen
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  4. M. L. Berumen
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  5. N. J. de Voogd
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Corresponding author

Correspondence to D. F. R Cleary.

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Electronic Supplementary Material

Supplementary Fig. 1

Location of the sampling area in the Red Sea. (PDF 857 kb)

Supplementary Fig. 2

Underwater photographs of all species sampled in the present study: (A) Xestospongia testudinaria, (B) Chalinula sp., (C) Petrosia elephantotus, (D) Topsentia aqabaensis, (E) Negombata magnifica, (F) Ectyoplasia coccinea, (G) Stylissa carteri, (H) Cinachyrella sp., (I) Dactylospongia metachromia, (J) Hyrtios sp., (K) Aplysinella rhax, (L) Leucetta chagosensis, (M) Ptilocaulis sp. (N) Luffariella variabilis, (O) Siphonogorgia sp. and (P) Melithaea rubrinodis. (PNG 10320 kb)

High Resolution Image (TIFF 14403 kb)

Supplementary Fig. 3

Ordination showing the third and fourth axes of the principal coordinates analysis (PCO) of OTU composition. In fig. 4a, light grey symbols represent operational taxonomic unit (OTU) scores with the symbol size proportional to their abundance (number of sequence reads). In fig. 4b, the colour of the symbol indicates the taxonomic affiliation. HMA sponges: Cs - Chalinula sp., Dm - Dactylospongia metachromia, Hy - Hyrtios sp., Lv - Luffariella variabilis, Pe - Petrosia elephantotus and Xt - Xestospongia testudinaria, LMA sponges: Ar - Aplysinella rhax, Ec - Ectyoplasia coccinea, Nm - Negombata magnifica, Cn - Cinachyrella sp., Ps - Ptilocaulis sp.., Sc - Stylissa carteri and Ta - Topsentia aqabaensis, calcareous sponge: Lc - Leucetta chagosensis, octocorals: Mr - Melithaea rubrinodis and Sg - Siphonogorgia sp., Sd - sediment and Wt – seawater. The third and fourth axes explain an additional 14% of the variation in composition. (PDF 1266 kb)

Supplementary Fig. 4

Relative abundance of the most abundant phyla in the demosponges Cs - Chalinula sp., Dm - Dactylospongia metachromia, Hy - Hyrtios sp., Lv - Luffariella variabilis, Pe - Petrosia elaphantotus and Xt - Xestospongia testudinaria, Ar - Aplysinella rhax, Ec - Ectyoplasia coccinea, Nm - Negombata magnifica, Pt - Cinachyrella sp., Ps - Ptilocaulis sp., Sc - Stylissa carteri and Ta - Topsentia aqabaensis, the calcareous sponge: Lc - Leucetta chagosensis, octocorals: Mr - Melithaea rubrinodis and Sg - Siphonogorgia sp., Sd - sediment and Wt - seawater (PDF 10 kb)

Supplementary Fig. 5

Rarefied richness of the demosponge species Cs - Chalinula sp., Dm - Dactylospongia metachromia, Hy - Hyrtios sp., Hr - Luffariella variabilis, Pe - Petrosia elaphantotus and Xt - Xestospongia testudinaria, Ar - Aplysinella rhax, Ec - Ectyoplasia coccinea, Nm - Negombata magnifica, Pt - Cinachyrella sp., Ps - Ptilocaulis sp., Sc - Stylissa carteri and Ta - Topsentia aqabaensis, the calcareous sponge: Lc - Leucetta chagosensis, the octocorals: Mr - Melithaea rubrinodis and Sg - Siphonogorgia sp., Sd - sediment and Wt - seawater. (PDF 111 kb)

Supplementary Table 1

List of samples used in the present study including the biotope, species and location. The relative percentages of the most abundant phyla, classes and orders are given as is the dominance (Dom; relative abundance of the most abundant OTU), Dom3 (relative abundance of the three most abundant OTUs), rarefied richness (Richness), Pielou’s J (J) and Shannon’s H′ diversity index (H). NCBI SRA metadata includes library_ID, study, Bioproject, accession, Biosample, seq_meth, library_strategy, library_source, library_layout, investigation_type, title, organism, project_name, lat_lon, geo_loc_name, collection_date, biome, feature, material and env_package. (XLS 98 kb)

Supplementary Table 2

Number of sequences and OTUs recorded for all phyla in the present study based on the Silva 128 database. (XLS 11 kb)

Supplementary Table 3

The number of phyla, orders and classes recorded in each biotope. (XLS 7 kb)

Supplementary Table 4

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 468 kb)

Supplementary Table 5

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. (XLS 1381 kb)

Supplementary Table 6

List of abundant (≥ 2500 sequence reads) OTUs and closely related organisms identified using BLAST search. OTU: OTU number; Sum: number of sequence reads; 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 18 kb)

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Cleary, D.F.R., Polónia, A., Reijnen, B. et al. Prokaryote Communities Inhabiting Endemic and Newly Discovered Sponges and Octocorals from the Red Sea. Microb Ecol 80, 103–119 (2020). https://doi.org/10.1007/s00248-019-01465-w

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