Abstract
Purpose
Assess microeukaryote community composition in seawater and sponge samples from Taiwanese coral reefs.
Methods
In the present study, we used Illumina sequencing to explore the microeukaryote communities of seven biotopes (six sponge species and seawater) sampled in the Penghu archipelago of Taiwan.
Result
Microeukaryote communities were dominated by Dinoflagellates with Dinophyceae and Syndiniales well represented in all biotopes. Other abundant taxa included metazoa, red and green algae and Radiolaria. The only significant differences were a significantly higher relative abundance of Picobiliphyta and Stramenopiles_X in seawater and Metamonada in the sponge Acanthostylotella cornuta. There was also a significant difference in composition among biotopes with samples from sponges and seawater forming distinct clusters. There was, however, no congruence between prokaryote and microeukaryote community composition. After removing all OTUs < 100 sequences, more than 90% of remaining OTUs representing > 99.5% of sequences were shared between sponge and seawater samples.
Conclusion
This data in the present study would appear to suggest that marine microeukaryote communities in sponges are largely derived from the surrounding seawater. Abundant OTUs were also related to organisms previously retrieved from seawater. A number of these OTUs though had relatively low sequence similarity to organisms in GenBank suggesting that more research of the microeukaryote communities in the Penghu archipelago may yield novel organisms in this relatively unexplored area.
References
Annenkova NV, Lavrov DV, Belikov SI (2011) Dinoflagellates associated with freshwater sponges from the ancient Lake Baikal. Protist 162:222–236. https://doi.org/10.1016/j.protis.2010.07.002
Bell J (2008) The functional roles of marine sponges. Estuar Coast Shelf Sci 79:341–353. https://doi.org/10.1016/j.ecss.2008.05.002
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
Chaib De Mares M, Sipkema D, Huang S, Bunk B, Overmann J and van Elsas JD (2017) Host specificity for bacterial, archaeal and fungal communities determined for high- and low-microbial abundance sponge species in two genera. Front. Microbiol 8:2560. https://doi.org/10.3389/fmicb.2017.02560
Cleary DFR, Polónia ARM (2018) Bacterial and archaeal communities inhabiting mussels, sediment and water in Indonesian anchialine lakes. Antonie Van Leeuwenhoek 111:237–257. https://doi.org/10.1007/s10482-017-0944-1
Cleary DFR, Polónia ARM, de Voogd NJ (2018) Bacterial communities inhabiting the sponge Biemna fortis, sediment and water in marine lakes and the open sea. Microb Ecol 76:610–624. https://doi.org/10.1007/s00248-018-1156-6
Coelho FJRC, Cleary DFR, Gomes NCM, Pólonia ARM, Huang YM, Liu LL, de Voogd NJ (2018) Sponge prokaryote communities in Taiwanese coral reef and shallow hydrothermal vent ecosystems. Microb Ecol 75:239–254. https://doi.org/10.1007/s00248-017-1023-x
Diaz MC, Rützler K (2001) Sponges: an essential component of Caribbean coral reefs. Bull Mar Sci 69:535–546
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998
Fan L, Reynolds D, Liu M, Stark M, Kjelleberg S, Webster NS, Thomas T (2012) Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proc Natl Acad Sci U S A 109:E1878–E1887. https://doi.org/10.1073/pnas.1203287109
Gómez F (2012) A quantitative review of the lifestyle, habitat and trophic diversity of dinoflagellates (Dinoflagellata, Alveolata). Syst Biodivers 10:267–275
González-Pech RA, Ragan MA, Chan CX (2017) Signatures of adaptation and symbiosis in genomes and transcriptomes of Symbiodinium. Sci Rep 7:15021. https://doi.org/10.1038/s41598-017-15029-w
Guillou L, Bachar D, Audic S et al (2013) The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote Small Sub-Unit rRNA sequences with curated taxonomy. Nucleic Acids Res 41(Database issue):D597–D604. https://doi.org/10.1093/nar/gks1160
Hentschel U, Usher KM, Taylor MW (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55:167–177
Hentschel U, Piel J, Degnan SM, Taylor MW (2012) Genomic insights into the marine sponge microbiome. Nat Rev Microbiol 10:641–654
Hochmuth T, Niederkrüger H, Gernert C, Siegl A, Taudien S, Platzer M, Crews P, Hentschel U, Piel J (2010) Linking chemical and microbial diversity in marine sponges: possible role for poribacteria as producers of methyl-branched fatty acids. Chembiochem 11:2572–2578. https://doi.org/10.1002/cbic.201000510
Huang YM, de Voogd NJ, Cleary DFR, Li T-H, Mok HK, Ueng JP (2016) Biodiversity pattern of subtidal sponges (Porifera: Demospongiae) in the Penghu Archipelago (Pescadores), Taiwan. J Mar Biol Assoc UK 96:417–427
Maldonado M, Aguilar R, Bannister RJ, Bell D, Conway KW, Dayton PK, Díaz C, Gutt J, Kelly M et al (2016) Sponge grounds as key marine habitats: a synthetic review of types, structure, functional roles, and conservation concerns. Marine Animal Forests. Springer, Berlin. https://doi.org/10.1007/978-3-319-17001-5_24-1
Piel J (2009) Metabolites from symbiotic bacteria. Nat Prod Rep 26:338–362
Price DC, Bhattacharya D (2017) Robust Dinoflagellata phylogeny inferred from public transcriptome databases. J Phycol 53:725–729
Quast C et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41(D1):D590–D596
R Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna 3-900051-07-0. http://www.R-project.org
Ramsby BD, Hill MS, Thornhill DJ, Steenhuizen SF, Achlatis M, Lewis AM, LaJeunesse TC (2017) Sibling species of mutualistic Symbiodinium clade G from bioeroding sponges in the western Pacific and western Atlantic oceans. J Phycol 53:951–960. https://doi.org/10.1111/jpy.12576
Rodríguez-Marconi S, De la Iglesia R, Díez B, Fonseca CA, Hajdu E, Trefault N (2015) Characterization of bacterial, archaeal and eukaryote symbionts from antarctic sponges reveals a high diversity at a three-domain level and a particular signature for this ecosystem. PLoS One 10:e0138837. https://doi.org/10.1371/journal.pone.0138837
Stoeck T, Bass D, Nebel M, Christen R, Jones MD, Breiner HW, Richards TA (2010) Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol Ecol 19:21–31. https://doi.org/10.1111/j.1365-294X.2009.04480.x
Strehlow B, Friday S, McCauley M, Hill M (2016) The potential of azooxanthellate poriferan hosts to assess the fundamental and realized Symbiodinium niche: evaluating a novel method to initiate Symbiodinium associations. Coral Reefs 35:1201–1212. https://doi.org/10.1007/s00338-016-1465-5
Swierts T, Cleary DFR, de Voogd NJ (2018) Biogeography of prokaryote communities in closely related giant barrel sponges across the Indo-Pacific. FEMS Microbiol Ecol 94(12):fiy194. https://doi.org/10.1093/femsec/fiy194
Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347
Wecker P, Fournier A, Bosserelle P, Debitus C, Lecellier G, Berteaux-Lecellier V (2015) Dinoflagellate diversity among nudibranchs and sponges from French Polynesia: insights into associations and transfer. C R Biol 338:278–283. https://doi.org/10.1016/j.crvi.2015.01.005
Acknowledgements
Support in the field and lab was provided by Julian Cleary, Floris Cleary, Yusheng Huang, Kate, Ana R.M. Polónia and Nicole J de Voogd.
Funding
Financial support was provided to CESAM (UID/AMB/50017 – POCI-01-0145-FEDER-007638) and for the project LESS CORAL (PTDC/AAC-AMB/115304/2009) by FCT/MEC through national funds, and co-funding by FEDER, within the PT2020 Partnership Agreement and Compete 2020.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author declares that he has no conflict of interest.
Research involving human participants and/or animals
This article does not contain any studies with human participants or laboratory animals.
Informed consent
Not applicable.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Supplementary Figure 1
Relative abundance of the most abundant microeukaryote higher taxa in sponges: Ac - Agelas cavernosa, Ar - Acanthostylotella cornuta, He - Hyrtios erectus, Xt - Xestospongia testudinaria, Echinodictyum asperum, Sc - Stylissa carteri, Su - Suberites diversicolor and Wt - water. (PDF 6.94 kb)
Supplementary Figure 2
Relative abundance of significantly discriminating OTUs between pairs of biotopes identified using Simper analysis (P < 0.001) and colour-coded according to microeukaryote taxon for Ac - Agelas cavernosa, Ar - Acanthostylotella cornuta, He - Hyrtios erectus, Xt - Xestospongia testudinaria, Ea - Echinodictyum asperum, Sc - Stylissa carteri, Su - Suberites diversicolor and Wt – water. The circle size of the OTU is proportional to the mean percentage of sequences per sample as indicated by the symbol legend in the bottom right corner. (PDF 66.6 kb)
Supplementary Figure 3
Heatmap showing the abundance of abundant microeukaryote OTUs (≥ 4000 sequences). The heatmap was generated using the function heatmap2() in the R package gplots (http://www.cran.r-project.org/). The OTUs were log-transformed and clustered according to their occurrence by UPGMA hierarchical clustering. Sponge species: Ac - Agelas cavernosa, Ar - Acanthostylotella cornuta, He - Hyrtios erectus, Xt - Xestospongia testudinaria, Ea - Echinodictyum asperum, Sc - Stylissa carteri, Su - Suberites diversicolor and Wt - water. (PDF 11.9 kb)
Supplementary Table 1
A summary of the samples collected is presented study including the name of the site, the location of the site in the northern or southern Penghu islands, the GPS coordinates, the biotope (host species, sediment or seawater), order and family of the host species. (XLS 20.5 kb)
Supplementary Table 2
Results of emmeans analysis showing pairwise comparisons of differences in the relative abundances of selected eukaryote higher taxa and the percentage of OTUs100 recorded in seawater as a percentage of total OTUs100 (WtToPr) between biotopes based on the ‘fdr’ test. Estimate (Estimated marginal means), SE (standard error), P (probability), Sig. (Significance): * 0.01 < Pr < 0.05 ** 0.001 < Pr < 0.01; *** Pr < 0.001. Variable: the dependent variable, Contrast: Contrasts between pairs of biotopes, SE: standard error. (XLS 78.5 kb)
Supplementary Table 3
Results of Simper analysis showing the contribution of microeukaryote OTUs to differences in similarity between pairs of biotopes. Contrast: contrasts between pairs of biotopes. Average: average contribution to overall dissimilarity. Sd: Standard deviation of contribution. Ratio: Average to sd ratio. Ava, Avb: average abundances per biotope. CumSum: ordered cumulative contribution. P: permutation p value. OTUs that contributed significantly to differences are indicated by significance (Sig.): * 0.01 < P < 0.05 ** 0.001 < P < 0.01; *** P < 0.001. (XLS 340 kb)
Supplementary Table 4
List of abundant (≥ 4000 sequence reads) OTUs and closely related organisms identified using BLAST search. OTU: OTU number; Sum: number of sequence reads; Group: biotope or biotopes where the OTUs were mainly found; 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. In the Group column the abbreviations stand for sponge species: Ac - Agelas cavernosa, Ar - Acanthostylotella cornuta, He - Hyrtios erectus, Xt - Xestospongia testudinaria, Ea - Echinodictyum asperum, Sc - Stylissa carteri, Su - Suberites diversicolor and Wt – seawater. (XLS 13.5 kb)
Rights and permissions
About this article
Cite this article
Cleary, D.F.R. A comparison of microeukaryote communities inhabiting sponges and seawater in a Taiwanese coral reef system. Ann Microbiol 69, 861–866 (2019). https://doi.org/10.1007/s13213-019-01476-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13213-019-01476-5