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Sponges and their microbiomes in clean and polluted habitats

Marta Turon1, Leire Garate1, Xavier Triadó-Margarit1, Joan Cáliz1 and Maria J. Uriz1*
  • 1 Centre d'Estudis Avançats de Blanes (CEAB-CSIC), Spain

Introduction Microbes have been inevitable intimate partners of sponges since the Pre-Cambrian (1). The prokaryote-eukaryote relationship is so tight in sponges that the attempts to culture sponge cells or symbiotic bacteria separately have systematically failed. Moreover, bacteria represent more tan 50% in volume of the microbial-sponge holobiont in some sponge species (2). Thus, it is hard to envisage the causes of sponge success or failure without considering its accompanying bacterial microbiome. Indeed unbalancing of their microbial symbiosis has been considered to trigger extensive mass mortalities in the Mediterranean (3) and Red Sea (4). Conversely, the purported sponge benefits from their associations with microbes have so far only rarely been reported (5,6). In this study, we address the effect of eutrophication on sponges and their associated microbiomes in a tropical area, which offered contrasting conditions at short geographical distances. Methods Sponge sampling was performed along 25 m long, transect lines, randomly placed on three differentiated habitats of Nha Trang Bay (Vietnam): rocky vertical walls, well-preserved coral reefs and polluted coral reefs. Fragments of ca. 3 cm2 of the 208 sponges crossed by the metric tape were collected and identified by molecular markers and morphological features afterwards. The microbiome from the most abundant sponges was analyzed by 16S-tag sequencing (Illumina platform) using the primers 564F and 785R at the MrDNA laboratory (Texas). The statistical test of Anosim was used for assessing differences in bacterial diversity among habitats and species. IndVal tests were performed to detect fidelity and abundance of the most abundant bacterial OTUS to any of the three habitats explored. Results and Discussion Sampling and study site The three different habitats showed differences in terms of sponge diversity and abundance. Most species were ambient-specific and only two species were shared by three sampled habitats: Gellioides cf. gracilis and Clathria cf. tuberosa. The latter, however, was most abundant in coral reefs. The rocky substrate showed the highest sponge abundance and provided 98 samples belonging to 42 species with most of the individuals encrusting and small. Sponges from coral reefs showed significant differences between the well preserved and the highly eutrophic sites, with a higher species richness in the former (29 vs. 15 species, respectively). In terms of abundance, however, the highly impacted coral reef showed the highest sponge coverage. Morevoer, the eutrophic zone was mostly dominated by two species Amphimedon sp and Clathria cf.tuberosa, which accounted for more that 50% of the specimens sampled. Microbiome analysis After quality check, dereplication and chimera filtering, a total of 9327 bacterial OTUs were clustered at a 97% sequence identity from the more abundant 20 sponge species. A total of 39 different bacterial phyla were recorded, with Proteobacteria (73.5%), Chloroflexi (3.2%), Actinobacteria (3.9%) and Acidobacteria (3.4%) being the most abundant. No significant differences in qualitative and quantitative diversity indices among habitats were retrieved whereas bacteria diversity mostly depended on the sponge species with Shannon diversity indices (H’) ranging from 4.6 to 1.6. Suberea cf. laboutei, Niphates sp. and Aaptos suberitoides, showed the highest H’ values and Terpios sp., Amphimedon sp and Antho sp. the lowest. Microbiome variation at any taxonomical level was in general low among sponge replicates except in a few of cases, which merit further investigation. Clustering sponge individuals as a function of microbiome similarity retrieved monospecific clades for Dysidea sp., Antho sp. Haliclona spp., Amphimedon sp., Clathria cf.tuberosa, Gellioides cf.gracilis, Monanchora unguiculata, Aaptos suberitoides, Suberea cf labutei and Biemna sp. IndVal analyses detected the phylum Rhodobactereacea significantly associated (p-val: 0.01) to those species proliferating in the eutrophic habitat. Rhodobactereacea includes several families with chemotrophic anaerobic metabolisms, which may be able to oxidize the Hydrogen Sulfide compounds that thrive in eutrophic environments. The particular abundance of Rhodobactereacea in sponges adapted to live in eutrophic habitats points to the sponge microbiomes as drivers of sponge adaptation to get over eutrophication pressures. Conclusions We conclude that sponge microbiomes are mainly species-specific and do not experience significant changes as a function of the habitat characteristics, what highlights the strength of these evolutionary fixed symbioses. However, only species that harbor particular microbiomes seem to be able to colonize eutrophic environments thanks to the ability of the symbiotic bacteria to cope with certain noxious components of the eutrophic waters.

Acknowledgements

This study was supported by the Spanish Ministry of Science and Innovation through the project MarSymbiOmics (CTM2013-43287-P).

References

1) Wilkinson, C. R. 1984. Inmunological evidences for the Precambrian origin of bacterial symbioses in marine sponges. Proc. R. Soc. Lond. B 220: 509–517.
2) Uriz MJ, Agell,G, Blanquer A, Turon X, Casamayor EO (2012) Endosymbiotic calcifying bacteria: a new cue to the origin of calcification in Metazoa?. Evolution. Doi:10.1111/j.1558-5646.2012.01676.x
3) Webster NS, Xavier JR, Freckelton M,Motti CA, Cobb R (2008) Shifts in microbial and chemical patterns within the marine sponge Aplysina aerophoba during a disease outbreak. Environ Microbiol 10:3366–3376.
4) Gao ZM, Wang Y, Lee OO, Tian RM, Wong YH, Bougouff S, Batang Z, Al-Suwailem A, Lafi FF, Bajic VB, Qian PY (2014) Pyrosequencing reveals the microbial communities in the red sea sponge Carteriospongia foliascens and their impressive shifts in abnormal tissues. Microbial Ecology 68:621–632.
5) Garate L, Blanquer A, Uriz MJ (2015) Calcareous spherules produced by intracelular symbiotic bacteria protect the sponge Hemimycale columella from predation better than secondary metabolites. Mar Ecol Prog Ser 523: 81–92
6) De Voogd NJ, Cleary DFR, Plónia ARM, Gomes NCM (2015) Bacterial community composition and predicted functional ecology of sponges, sediment and seawater from the thousand islands reef complex, West Java, Indonesia. FEMS Micro. Ecol 91. Doi: 10.1093/femsec/fiv019

Keywords: Sponges, Microbiome profiling, Symbiosis, Eutrophication, coral reefs, Indo-Pacific

Conference: XIX Iberian Symposium on Marine Biology Studies, Porto, Portugal, 5 Sep - 9 Sep, 2016.

Presentation Type: Oral Presentation

Topic: 1. ECOLOGY, BIODIVERSITY AND VULNERABLE ECOSYSTEMS

Citation: Turon M, Garate L, Triadó-Margarit X, Cáliz J and Uriz MJ (2016). Sponges and their microbiomes in clean and polluted habitats. Front. Mar. Sci. Conference Abstract: XIX Iberian Symposium on Marine Biology Studies. doi: 10.3389/conf.FMARS.2016.05.00042

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Received: 27 Apr 2016; Published Online: 02 Sep 2016.

* Correspondence: Dr. Maria J Uriz, Centre d'Estudis Avançats de Blanes (CEAB-CSIC), Blanes, Girona, 17300, Spain, iosune@ceab.csic.es