Hologenome Analysis of Two Marine Sponges with Different Microbiomes
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Ryu et al. BMC Genomics (2016) 17:158 DOI 10.1186/s12864-016-2501-0 RESEARCH ARTICLE Open Access Hologenome analysis of two marine sponges with different microbiomes Taewoo Ryu1,2,12*, Loqmane Seridi1,2, Lucas Moitinho-Silva3,MatthewOates4,YiJinLiew2,5, Charalampos Mavromatis1,2, Xiaolei Wang6,7, Annika Haywood2, Feras F. Lafi2,8, Marija Kupresanin1,2, Rachid Sougrat9, Majed A. Alzahrani6,7, Emily Giles2,YanalGhosheh1,2, Celia Schunter1,2, Sebastian Baumgarten2,5,MichaelL.Berumen2,5,XinGao6,7, Manuel Aranda2,5,SylvainForet10, Julian Gough4, Christian R. Voolstra2,5, Ute Hentschel11 and Timothy Ravasi1,2* Abstract Background: Sponges (Porifera) harbor distinct microbial consortia within their mesohyl interior. We herein analysed the hologenomes of Stylissa carteri and Xestospongia testudinaria, which notably differ in their microbiome content. Results: Our analysis revealed that S. carteri has an expanded repertoire of immunological domains, specifically Scavenger Receptor Cysteine-Rich (SRCR)-like domains, compared to X. testudinaria.Onthemicrobialside, metatranscriptome analyses revealed an overrepresentation of potential symbiosis-related domains in X. testudinaria. Conclusions: Our findings provide genomic insights into the molecular mechanisms underlying host-symbiont coevolution and may serve as a roadmap for future hologenome analyses. Keywords: Sponge, Stylissa carteri, Xestospongia testudinaria, Innate immune system, Host, Microbial symbionts, Hologenome Background tropical reefs to the cold deep sea and are even present in Microbial symbionts are being increasingly recognised as freshwater lakes and streams. As sessile filter feeders, they deeply integral components of multicellular organisms pump many thousands liters of water per day through the that affect core host functions such as development, im- aquiferous canal system that is embedded within the munity, nutrition, and reproduction [1]. The holobiont sponge body and are constantly exposed to a plethora of (synonym with “metaorganism”, and defined as the host microorganisms from the environment [5]. Many species organism and its collective microbial community) [2] is are colonised by dense and diverse microbial consortia thus considered a biological unit of natural selection that are contained extracellularly within the mesohyl (the “hologenome theory”) [3]. However, the molecular matrix (“high microbial abundance” (HMA)), while other mechanisms (e.g., immune system evasion and toler- species are nearly devoid of microorganisms (“low micro- ance) that have resulted in these symbiotic partnerships bial abundance” (LMA)) [6–8]. are poorly understood. To investigate factors involved in sponge-microbe inter- Sponges (Porifera) represent one of the oldest, still ex- actions, we herein sequenced and analysed hologenome tant animal phyla. Fossil evidence dating back 580 million data including genome, transcriptome, and metatranscrip- years ago shows their existence in the Precambrian long tome of S. carteri (an LMA sponge and hereafter referred before the radiation of all other animal phyla [4]. Sponges to as “SC”)andX. testudinaria (an HMA sponge and are globally distributed in all aquatic habitats from warm hereafter referred to as “XT”) (Fig. 1, Additional file 1 and Additional file 2). These two sponges were collected from * Correspondence: TaewooRyu16@apcc21.org; timothy.ravasi@kaust.edu.sa the same habitat, which ensured systematic comparison 1KAUST Environmental Epigenetic Program (KEEP), King Abdullah University by minimizing environmental effect such as different of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia planktons and temperature. SC is the first species in the 2Division of Biological and Environmental Sciences & Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, order Halichondrida to have its genome sequenced while Kingdom of Saudi Arabia XT (order Haplosclerida) is the first HMA sponge to have Full list of author information is available at the end of the article © 2016 Ryu et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Konstanzer Online-Publikations-System (KOPS) URL: http://nbn-resolving.de/urn:nbn:de:bsz:352-2-hmx9j75dpgpw8 Ryu et al. BMC Genomics (2016) 17:158 Page 2 of 11 Fig. 1 Sponge species. Underwater images of Stylissa carteri (a) and Xestospongia testudinaria (b) taken by Michael L. Berumen its genome sequenced [8]. Thus, our work provides a immunity,”“antimicrobial peptides,” and “antibacterial”) unique and valuable resource for future studies. in functional annotations of the SUPERFAMILY data- base [13] (Fig. 2a and Additional file 6). We also in- Results and discussion cluded Amphimedon queenslandica (hereafter referred Genome assembly and gene annotation to as “AQ”) in this analysis because its genome has been Our assemblies of the SC and XT genomes yielded stably annotated [9] and also because its status with re- 97,497 and 97,640 scaffolds with base-level coverages of spect to microbial load is well known (LMA, Sandie 109 X and 59 X, respectively (Additional file 3). The esti- Degnan, personal communication). Furthermore, overall mated genome sizes obtained from our assemblies were gene contents of AQ are comparable to our studied comparable to experimentally determined genome sizes sponges: among 30,060 gene models for AQ,17,567genes measured by flow cytometry (386.31 and 161.37 Mbp for contained 32,326 SUPERFAMILY domains (28,027 and SC and XT, respectively, see Methods). 26,967 and 22,337 29,156 SUPERFAMILY domains from 17,074 and 17,664 gene models of high quality were predicted covering 94.5 genes for SC and XT, respectively. Additional file 4). Other and 94.3 % of the core eukaryotic genes for SC and XT,re- sponges with public transcript models were excluded due spectively (see Methods). Comparison to publicly available to incompleteness of gene models as shown in Additional sponge gene models from draft genomes or transcrip- file 4 and lack of exact status of LMA and HMA. tomes [9–11] shows that our gene models have reasonable Our results revealed that there had been a striking ex- quality in terms of the number of coding sequences pansion of the Scavenger Receptor Cysteine-Rich (SRCR)- (CDSs), the representation of core eukaryotic gene set like domain in the three tested sponges compared to all [12], the number of genes with protein domains, and the other eukaryotes compiled in the SUPERFAMILY data- number of protein domains (Additional file 4). base (see Additional file 6 for selected taxa). One known function of SRCR-like domains is recognition of large and Expansion of innate immunological domains in sponge diverse patterns of macromolecules (e.g., modified low- hosts density lipoprotein; LDL) on microbial surfaces and en- We checked for protein domains that were unusually hancement of the phagocytic clearance of microbes [7]. In over- or under-represented in the studied sponges com- mammals, malfunctions in SRCR-like-domain-containing pared to other eukaryotes compiled in the SUPERFAM- proteins have been linked to diseases and bacterial/viral ILY database [13]. Most protein domains were neither infections [15]. It has been suggested that a protein con- over- nor under-represented, indicating that our gene taining this domain in the Mediterranean sponge (Petrosia models are comparable to those of other eukaryotes ficiformis) may function in the recognition of photosym- (Additional file 5). Both sponges (particularly SC) bionts [16]. We found that the SC genome contains 2166 showed substantial expansions of immunological and re- SRCR-like domains, which is the highest number found ceptor domains (Additional file 5) [14]. We focused our among the 427 eukaryotes compiled in the SUPERFAM- analysis on protein domains relevant to host-microbe in- ILY database (average, 28 copies). Interestingly, the next- teractions by using four keywords (“symbio,”“innate highest known copy number for this domain family is Ryu et al. BMC Genomics (2016) 17:158 Page 3 of 11 Fig. 2 Domain expansion and contraction in LMA vs. HMA sponges. Innate immune- and symbiosis-related protein domains were selected from the functional annotation. a The number of times a domain occurs in each genome. Shown are domains found ≥ 1.5 times more in SC compared to XT, or vice versa. AQ is included for comparison. The domain occurrence is highly correlated in the LMA sponges (AQ and SC; Pearson correlation coefficient = 0.92). The numbers of genes containing the domains are shown in the bracket. b The co-occurrence of innate immune domains in sponges. Nodes represent domains, while the numbers above the edges indicate the number of proteins in which the two domains co-occur for each sponge (the color key is shown at the bottom-left). Each node size is proportional to the number of outgoing edges. Edges are shown only when the domain pairs were observed ≥ 5 times in ≥ 1species found in AQ, followed closely by the sea urchin, Strongylo- three sponges yielded a large number