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Compositional Analysis of Archaeal Communities in High and Low Microbial Abundance Sponges in the Misool Coral Reef System, Indonesia

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Compositional Analysis of Archaeal Communities in High and Low Microbial Abundance Sponges in the Misool Coral Reef System, Indonesia Marine Biology Research ISSN: 1745-1000 (Print) 1745-1019 (Online) Journal homepage: http://www.tandfonline.com/loi/smar20 Compositional analysis of archaeal communities in high and low microbial abundance sponges in the Misool coral reef system, Indonesia Ana Rita Moura Polónia, Daniel Francis Richard Cleary, Francisco José Riso da Costa Coelho, Leontine E. Becking, Nicole Joy de Voogd, Abdul Hamid A. Toha & Newton Carlos Marcial Gomes To cite this article: Ana Rita Moura Polónia, Daniel Francis Richard Cleary, Francisco José Riso da Costa Coelho, Leontine E. Becking, Nicole Joy de Voogd, Abdul Hamid A. Toha & Newton Carlos Marcial Gomes (2018) Compositional analysis of archaeal communities in high and low microbial abundance sponges in the Misool coral reef system, Indonesia, Marine Biology Research, 14:6, 537-550, DOI: 10.1080/17451000.2018.1498977 To link to this article: https://doi.org/10.1080/17451000.2018.1498977 Published online: 03 Aug 2018. Submit your article to this journal Article views: 45 View Crossmark data Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=smar20 MARINE BIOLOGY RESEARCH 2018, VOL. 14, NO. 6, 537–550 https://doi.org/10.1080/17451000.2018.1498977 ORIGINAL ARTICLE Compositional analysis of archaeal communities in high and low microbial abundance sponges in the Misool coral reef system, Indonesia Ana Rita Moura Polóniaa, Daniel Francis Richard Cleary a, Francisco José Riso da Costa Coelhoa, Leontine E. Beckingb,c,d, Nicole Joy de Voogdb,e, Abdul Hamid A. Tohaf and Newton Carlos Marcial Gomesa aDepartment of Biology, CESAM, Universidade de Aveiro, Aveiro, Portugal; bMarine Biodiversity Group, Naturalis Biodiversity Center, Leiden, the Netherlands; cMarine Animal Ecology, Wageningen, the Netherlands; dWageningen Marine Research, Den Helder, the Netherlands; eDepartment of Environmental Biology, Institute of Environmental Sciences (CML), University of Leiden, Leiden, the Netherlands; fFisheries Department, Papua University, Manokwari, Indonesia ABSTRACT ARTICLE HISTORY The high/low microbial abundance (HMA/LMA) dichotomy in sponges has been the subject of Received 6 May 2017 several studies over recent years, but few studies have analysed this dichotomy in terms of the Accepted 25 June 2018 sponge archaeal community and function. Using a 16S rRNA gene barcoded pyrosequencing Published online 3 August approach and predictive functional analysis (PICRUSt) we compared the archaeal 2018 composition, richness and predicted function of one HMA sponge (Xestospongia testudinaria), SUBJECT EDITOR one LMA sponge (Stylissa carteri) and one sponge species of unknown microbial abundance Mathias Middelboe (Aaptos lobata). Although most of the archaeal sequences were assigned to the Crenarchaeota phylum, S. carteri had the highest percentage of sequences assigned to the KEYWORDS Euryarchaeota phylum. Variation among sponge species explained >85% of the variation in Archaea;16S rRNA gene; archaeal operational taxonomic unit (OTU) composition with each sponge species forming a Aaptos lobata; HMA; LMA; distinct cluster. There were significant differences in predicted PICRUSt profiles among PICRUSt sponge species, suggesting that archaeal communities present in the studied sponge species may perform different functions. X. testudinaria and A. lobata were similar both in terms of OTU and KEGG orthologues composition, which may indicate that A. lobata is a HMA sponge. Additionally, some of the most enriched functions seem to be related to traits associated with high and low microbial abundance sponges. carbon fixation); degradation of benzoic compounds; Introduction biosynthesis of secondary metabolites, antibiotics, Marine sponges are abundant, conspicuous sessile cofactors and vitamins; redox sensing and response filter-feeders which harbour exceptionally high (Thomas et al. 2010; Fan et al. 2012; Hentschel et al. microbial (Archaea, Bacteria, and Eukaryota) densities 2012). This functional repertoire benefits sponges by (Diaz and Rützler 2001) within their mesohyl (Moi- enhancing nutrient transfer; growth rates; aiding in tinho-Silva et al. 2014). By actively filtering large metabolic waste processing; and providing protection volumes of seawater, sponges contribute to benthic– against ultraviolet light and disease (Simpson 1984; pelagic coupling and to water column composition Hentschel et al. 2002; Holmes and Blanch 2007; Erwin alteration (e.g. secondary metabolite emanation, nutri- and Thacker 2008; Cebrian et al. 2011;Websterand ent transformations; e.g. Bell 2008;Hoffmann et al. Taylor 2012; Freeman et al. 2013). Additionally, these 2009; McMurray et al. 2014). microbial-mediated metabolic functions play important It has been assumed that part of the sponge func- ecological roles in coral reefs (e.g. Yahel et al. 2003; tional repertoire has its origin not in the sponge itself Hoffmann et al. 2009; de Goeij et al. 2013). Most but in its symbionts (e.g. Freeman and Thacker 2011; microbial community studies of coral reefs have, Ribes et al. 2012, 2015). Although not completely however, focused on bacterial communities and less understood, due to the lack of studies of cultured attention has been paid to archaeal communities. The endosymbionts, sponge-associated microorganisms same holds for sponge studies where the archaeal com- are likely involved in nutrient transport and utilization munities are still less studied, and thus less understood, (denitrification; nitrification, ammonium oxidation; than bacterial communities. CONTACT Ana Rita Moura Polónia [email protected] Department of Biology, CESAM, Universidade de Aveiro, Campus Universitário de San- tiago, 3810-193 Aveiro, Portugal The supplementary material for this article (Table SI, Figures S1–S4) is available at https://doi.org/10.1080/17451000.2018.1498977 © 2018 Informa UK Limited, trading as Taylor & Francis Group Published online 03 Aug 2018 538 A. R. M. POLÓNIA ET AL. Archaea members can dominate the microbial com- was slightly less abundant in HMA sponges. There are munity in some sponges; for example, in Dragmacidon conflicting results among studies as to which factors mexicana and Inflatella pellicula, Archaea account for better explain the microbial community composition more than 60% of all prokaryote cells (Preston et al. of sponges; and it remains uncertain which is the 1996; Jackson et al. 2013). Environmental factors may most important factor influencing sponge microbial influence the sponge archaeal community (Turque communities (host microbial abundance groups or et al., 2010), although there is some indication that host phylogeny; Blanquer et al. 2013; Schöttner et al. the sponge archaeal community is related to sponge 2013). phylogeny (Schmitt et al. 2008; Steger et al. 2008). The influence of microbial abundances in sponge Zhang et al. (2014), studied sympatric sponges from function remains largely unknown as well as the eco- the Mediterranean (collected in different seasons) and logical consequences of a functional HMA/LMA dichot- the Caribbean and showed specificity and persistence omy. Bayer et al. (2014b) suggested that the HMA/LMA of archaeal symbionts within sponge species. One of dichotomy extends to the functional gene level, the archaeal members most frequently associated however, few specificdifferences exist when individual with sponges belongs to the phylum Thaumarchaeota genes were inspected. Most of the studies of sponge (Brochier-Armanet et al. 2008). This phylum includes microbial HMA/LMA dichotomy have concentrated on members that are able to convert ammonium to bacterial communities, little is known about the exist- nitrite and fixCO2 through ammonia oxidation. These ence of an archaeal dichotomy between HMA and characteristics suggest that Archaea may play critical LMA sponges. roles in sponge hosts. These roles are likely linked In the present study, we assessed the composition with the sponge nitrogen metabolism and conse- of Archaea in three sponge species: the demosponges quently with the nitrogen cycle (Zhang et al. 2014). Stylissa carteri (Scopalinida: Scopalinidae; LMA; Giles However, the exact roles played by Archaea are still et al. 2013), Xestospongia testudinaria (Haplosclerida: largely unknown. Petrosiidae; HMA; Gloeckner et al. 2014) and Aaptos Sponge species differ substantially in terms of the lobata (Suberitida: Suberitidae; unknown microbial abundance of their microbial symbiont communities abundance), collected from three reef sites in the (e.g. Hentschel et al. 2003; Kamke et al. 2010; Bayer coral reef system of South East Misool, Papua, eastern et al. 2014a). While some species have a number of Indonesia. Our main goals were to compare archaeal microorganisms in the order of 109 cells per gram richness, composition and putative function between wet weight of sponge (‘high microbial abundance’– HMA and LMA sponges using a 16S rRNA gene bar- HMA) others have a number of microorganisms coded pyrosequencing approach and a predictive similar to that found in the surrounding seawater metagenomic approach. (‘low microbial abundance’– LMA), i.e. 105 to 106 cells per gram wet weight of sponge (Hentschel et al. 2012). This dichotomy is not only related to microbial Materials and methods abundance but also to sponge morphology and physi- Data collection ology, microbial diversity, microbial composition and microbial specificity (Erwin et al. 2015 and references Triplicate samples of Stylissa carteri, Aaptos lobata and therein). HMA sponges host highly
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