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Microbial Community Composition of Deep-Sea Corals from the Red Sea www.nature.com/scientificreports OPEN Microbial community composition of deep-sea corals from the Red Sea provides insight into functional Received: 30 November 2016 Accepted: 13 February 2017 adaption to a unique environment Published: 17 March 2017 Till Röthig*, Lauren K. Yum*, Stephan G. Kremb, Anna Roik & Christian R. Voolstra Microbes associated with deep-sea corals remain poorly studied. The lack of symbiotic algae suggests that associated microbes may play a fundamental role in maintaining a viable coral host via acquisition and recycling of nutrients. Here we employed 16 S rRNA gene sequencing to study bacterial communities of three deep-sea scleractinian corals from the Red Sea, Dendrophyllia sp., Eguchipsammia fistula, and Rhizotrochus typus. We found diverse, species-specific microbiomes, distinct from the surrounding seawater. Microbiomes were comprised of few abundant bacteria, which constituted the majority of sequences (up to 58% depending on the coral species). In addition, we found a high diversity of rare bacteria (taxa at <1% abundance comprised >90% of all bacteria). Interestingly, we identified anaerobic bacteria, potentially providing metabolic functions at low oxygen conditions, as well as bacteria harboring the potential to degrade crude oil components. Considering the presence of oil and gas fields in the Red Sea, these bacteria may unlock this carbon source for the coral host. In conclusion, the prevailing environmental conditions of the deep Red Sea (>20 °C, <2 mg oxygen L−1) may require distinct functional adaptations, and our data suggest that bacterial communities may contribute to coral functioning in this challenging environment. A growing number of studies support the notion that bacteria associated with multicellular hosts provide impor- tant functions related to metabolism, immunity, and environmental adaptation (among others)1. This might be of particular significance in ‘extreme’ environments, such as the deep sea. Nevertheless, only few studies investigated the diversity and function of bacteria associated with deep-sea corals. Similar to shallow corals2, deep-sea coral mucus stimulates microbial activity in the immediate vicinity of the coral host, suggestive of nutrient cycling via a microbial loop and thereby increasing ecosystem productivity3. However, deep-sea coral ecology is fundamen- tally different from the ecology of shallow-water corals. Deep-sea corals lack light, are exposed to elevated pres- sures, and usually reside at cold(er) temperatures4. Most importantly, they do not associate with photosynthetic algal symbionts in the genus Symbiodinium, and thereby lack a carbon source that provides the majority of the energetic requirements of shallow-water corals. Consequently, associated microbial communities of deep-sea corals are thought to play an essential role for host metabolism, e.g. by supplementing host feeding via fixing and recycling of nitrogen and carbon5–7. In support of this, in shallow-water corals increased bacterial diversity with increasing water depth has been suggested as a mechanism to aid nutrient acquisition8. Studies of Red Sea corals, along with those in the Persian/Arabian Gulf, are of interest in light of global climate change because corals in this region thrive at summer temperatures (> 31 °C) that are hostile for corals from other regions9,10. The tolerance to high temperature extends down to the depths of the Red Sea, where deep-sea corals are found at > 20 °C11. The discovery of deep-sea corals at this temperature prompted a reconsideration of environmental limitations of deep-sea corals, previously considered to be limited to temperatures of 4–14 °C4,12. Besides these unusual high temperatures, a study from the central Red Sea by Roder et al.11 reported higher salin- ity (40.5 PSU) and lower dissolved oxygen (1–2 mg L−1) levels, compared to other deep-sea coral environments. Red Sea Research Center, Division of Biological and Environmental Science and Engineering (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal 23955-6900, Saudi Arabia. *These authors contributed equally to this work. Correspondence and requests for materials should be addressed to C.R.V. (email: christian. [email protected]) SCIENTIFIC REPORTS | 7:44714 | DOI: 10.1038/srep44714 1 www.nature.com/scientificreports/ Dendrophyllia sp. E.fistula R.typus 6% 6% 17% 19% 1% 38% 38% 31% 7% 44% 4% 7% 12% 5% 4% 3% 1% 1% 4% 12% 9% 7% 1% 1% 17% 1% 2%1% 1% 100 ) 75 others Piscirickettsiaceae Rhodospirillaceae undances (% Vibrionaceae ab 50 unclassified (order Flavobacteriales) ve Pseudoalteromonadaceae Relati Moraxellaceae Pseudomonadaceae Rhodobacteraceae 25 Flavobacteriaceae unclassified (class Gammaproteobacteria) Alteromonadaceae unclassified (phylum Proteobacteria) 0 3 4 .1 .2 .3 .4 4 ter 2 ater 3 Water 1 Wa W yllia sp yllia sp yllia sp yllia sp R.typus 1 R.typus 2 R.typus 3 R.typus E.fistula 1 E.fistula 2 E.fistula E.fistula Dendroph Dendroph Dendroph Dendroph Figure 1. Bacterial community composition of deep-sea corals and seawater from the Red Sea on the bacterial family level (Greengenes database, bootstrap ≥60). Pie charts denote average bacterial abundance across replicates for the three coral species. The taxonomy bar plot denotes relative bacterial abundance across species replicates and seawater. Each color represents one of the 12 most abundant families (overall sequence count) in all samples. All other taxa are grouped under category ‘others’. To date, only few studies investigated microbial communities associated with deep-sea reef communities. At present, studies have focused on octocorals7,13–15 and two cold-water scleractinian corals, Lophelia pertusa and Madrepora oculata5,16–25. These studies support the presence of species-specific microbiomes7,14,23, but at the same time identified highly variable bacterial community structures depending on phenotype, spatial and temporal scales, and even on individual polyps within a colony5,18,19,21,23. To gain insight into bacterial community structure associated with deep-sea scleractinian corals from the Red Sea, we conducted a 16S rRNA gene survey on specimens from E. fistula, Dendrophyllia sp., and R. typus. We were interested to elucidate how bacterial association differs between coral hosts, and also, whether we find support for a bacterial contribution to functional adaptation to the distinct environment of the Red Sea. Results Microbial community composition of deep-sea corals and surrounding seawater. A total of 852,313 sequences were processed and, after filtering, yielded 554,088 sequences across 15 samples (i.e., 4 samples of Dendrophyllia sp., 4 samples of E. fistula, 4 samples of R. typus, and 1 water sample for each of the 3 collection sites). To evaluate bacterial community composition across samples, we classified all sequences to the family level (Fig. 1). The bacterial community composition of coral samples was markedly different from seawater samples that appeared similar across sampling sites (Fig. 1). Coral community composition differed in a species-specific manner with apparent within-species variation (Fig. 1). Differences and similarities within and between coral species and seawater. In order to identify differences in the bacterial community composition between different deep-sea corals, sequences were subsam- pled and clustered into OTUs (Operational Taxonomic Units) (Table 1). Species richness, i.e. the number of SCIENTIFIC REPORTS | 7:44714 | DOI: 10.1038/srep44714 2 www.nature.com/scientificreports/ No. of No. of Simpson Inverse Simpson Sample Name Sequences OTUs* Chao 1* Evenness* Index* Dendrophyllia sp. 1 20,984 682 1050 0.126 85.6 Dendrophyllia sp. 2 4,607 173 176 0.069 11.9 Dendrophyllia sp. 3 28,345 230 295 0.070 16.1 Dendrophyllia sp. 4 68,562 229 262 0.083 19.1 AVG 30,625 329 446 0.087 33.2 SD 27,168 237 406 0.027 35.1 E.fistula 1 58,909 657 899 0.067 44.3 E.fistula 2 21,485 589 839 0.079 46.7 E.fistula 3 10,830 318 451 0.019 6.1 E.fistula 4 33,871 337 468 0.010 3.2 AVG 31,274 475 664 0.044 25.1 SD 20,690 173 238 0.035 23.6 R. typus 1 12,664 452 675 0.026 11.9 R. typus 2 39,931 202 442 0.031 6.3 R. typus 3 63,947 241 586 0.020 4.7 R. typus 4 56,370 191 451 0.014 2.7 AVG 43,228 272 538 0.023 6.4 SD 22,708 122 112 0.007 3.9 Seawater1 45,931 265 506 0.024 6.4 Seawater2 32,959 244 482 0.019 4.6 Seawater3 54,693 358 599 0.045 16.0 AVG 44,528 289 529 0.029 9.0 SD 10,935 61 62 0.014 6.1 Table 1. Summary statistics of 16S rRNA-based bacterial community composition of deep-sea coral and seawater samples. *Based on subsampled sequences (n = 4,600). AVG = average; SD = standard deviation. different bacterial species present in each coral, was estimated using the Chao1 index26. Bacterial species richness estimates ranged from 176 to 1050 taxa for Dendrophyllia sp., from 451 to 899 for E. fistula, from 442 to 675 for R. typus, and from 482 to 599 for seawater. This indicates that species richness in corals was similar to that of the sur- rounding seawater. Simpson Evenness27 ranged from 0.069 to 0.126 for Dendrophyllia sp., from 0.010 to 0.079 for E. fistula, from 0.020 to 0.031 for R. typus, and from 0.019 to 0.045 for sea water. Species diversity (i.e. Inverse Simpson Index27) ranged between 11.9 and 85.6 for Dendrophyllia sp., 3.2 and 46.7 for E. fistula, 2.7 and 11.9 for R. typus, and 4.6 and 16.0 for sea water samples. The wide range of bacterial richness and diversity across coral species and in particular for Dendrophyllia sp.
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