Abstract
To address the metabolic potential of symbiotic Aquimarina spp., we report here the genome sequence of Aquimarina sp. strain EL33, a bacterium isolated from the gorgonian coral Eunicella labiata. This first-described (to our knowledge) animal-associated Aquimarina genome possesses a sophisticated repertoire of genes involved in drug/antibiotic resistance and biosynthesis.
GENOME ANNOUNCEMENT
The recently described Aquimarina genus (1), so far comprising 20 recognized species, encompasses primarily marine heterotrophic aerobic bacteria belonging to the metabolically plastic Flavobacteriaceae family (Bacteroidetes). Currently, there are only 10 Aquimarina genome sequences available in public databases (http://www.ncbi.nlm.nih.gov), all describing planktonic or alga-associated strains. Aquimarina species have also been retrieved from several animal hosts (2–5), but knowledge of their roles in association with metazoans is limited. To enable an inspection of the putative symbiotic features of the genus, we announce the nearly complete genome sequence of Aquimarina sp. strain EL33, a strain isolated from the gorgonian coral Eunicella labiata Thomson 1927. The host organism was sampled at ca. 18-m depth in the Atlantic Ocean, offshore of the Algarve region, South Portugal (36°58′47.2ʺN, 7°59′20.8ʺW). In the laboratory, host-derived microbial cell suspensions were prepared as described previously (6) and inoculated onto diluted (1:2) marine agar medium for 1 week at 18°C. Genomic DNA of strain EL33 was extracted and sequenced on an Illumina MiSeq platform, as performed elsewhere (7, 8). Sequence output was about 1.02 Gb, comprising 2 × 1,701,863 paired-end reads of 301 bp, corresponding to ca. 163× coverage of the genome. Sequence reads were assembled de novo into 20 contigs with the NGen DNA assembly software by DNAStar, Inc. Gene prediction and annotation were performed with the Rapid Annotation using Subsystem Technology (RAST) prokaryotic genome annotation server, version 2.0 (9).
The genome is composed of 6,270,711 bp, with a calculated G+C content of 32.9%. It possesses 5,530 coding sequences in addition to 40 tRNA and five rRNAs. Aquimarina sp. EL33 presents the highest 16S rRNA gene similarity (99.7%) with Aquimarina sp. Aq349, isolated from the marine sponge Sarcotragus spinosulus (6). Aquimarina megaterium XH134, isolated from surface seawater (10), is the closest described type strain (99.2% 16S rRNA gene similarity).
Aquimarina sp. EL33 possesses several genes involved in nutrient cycling (C, N, and S), suggesting versatile nutrient acquisition and utilization, in line with observations made for Aquimarina longa SW024 (11). For example, 19 chitinase-encoding genes (endochitinases EC 3.2.1.14) were found, indicating that strain EL33 is capable of degrading chitin, the most abundant polysaccharide in the oceans. Indeed, in vitro chitinolytic activity was shown for A. longa SW024 (11), which possesses seven chitinase-encoding genes.
The genome further reveals an elaborate arsenal of defense mechanisms. Thirty-five β-lactamase-encoding genes were identified, suggesting resistance of the strain to manifold β-lactam antibiotics. In addition, several genes encoding multidrug efflux pumps, drug transporters, and transition-metal cation binding proteins were detected, possibly enabling strain EL33 to cope with the activity of competing microorganisms and to persist in/on its host. Highlighting the potential antimicrobial activity of Aquimarina sp. EL33 is the presence of the lodAB operon responsible for the biosynthesis of marinocine, a lysin oxidase antimicrobial protein. Also, we observed at least two polyketide synthase (PKS)-encoding genes in the EL33 genome, corroborating earlier PCR-based detection of PKS genes across several strains of the genus (6).
Accession number(s).
The genome sequence of Aquimarina sp. EL33 has been deposited in the European Nucleotide Archive (ENA) under the accession numbers FLRG01000001 to FLRG01000020. The study Identification number is PRJEB14417.
Funding Statement
This work was partially funded by the Portuguese Foundation for Science and Technology (UID/Multi/04326/2013).
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Footnotes
Citation Keller-Costa T, Silva R, Lago-Lestón A, Costa R. 2016. Genomic insights into Aquimarina sp. strain EL33, a bacterial symbiont of the gorgonian coral Eunicella labiata. Genome Announc 4(4):e00855-16. doi:10.1128/genomeA.00855-16.
REFERENCES
- 1.Nedashkovskaya OI, Kim SB, Lysenko AM, Frolova GM, Mikhailov VV, Lee KH, Bae KS. 2005. Description of Aquimarina muelleri gen. nov., sp. nov., and proposal of the reclassification of Cytophaga latercula Lewin 1969 as Stanierella latercula gen. nov., comb. nov. Int J Syst Evol Microbiol 55:225–229. doi: 10.1099/ijs.0.63349-0. [DOI] [PubMed] [Google Scholar]
- 2.Nedashkovskaya OI, Vancanneyt M, Christiaens L, Kalinovskaya NI, Mikhailov VV, Swings J. 2006. Aquimarina intermedia sp. nov., reclassification of Stanierella latercula (Lewin 1969) as Aquimarina latercula comb. nov. and Gaetbulimicrobium brevivitae Yoon et al. 2006 as Aquimarina brevivitae comb. nov. and emended description of the genus Aquimarina. Int J Syst Evol Microbiol 56:2037–2041. doi: 10.1099/ijs.0.64155-0. [DOI] [PubMed] [Google Scholar]
- 3.Yoon B-J, You H-S, Lee D-H, Oh D-C. 2011. Aquimarina spongiae sp. nov., isolated from marine sponge Halichondria oshoro. Int J Syst Evol Microbiol 61:417–421. doi: 10.1099/ijs.0.022046-0. [DOI] [PubMed] [Google Scholar]
- 4.Park SC, Choe HN, Baik KS, Seong CN. 2012. Aquimarina mytili sp. nov., isolated from the gut microflora of a mussel, Mytilus coruscus, and emended description of Aquimarina macrocephali. Int J Syst Evol Microbiol 62:1974–1979. doi: 10.1099/ijs.0.032904-0. [DOI] [PubMed] [Google Scholar]
- 5.Zheng Y, Wang Y, Liu Y, Li W, Yu M, Zhang X-H. 2016. Aquimarina hainanensis sp. nov., isolated from diseased Pacific white shrimp Litopenaeus vannamei larvae. Int J Syst Evol Microbiol 66:70–75. doi: 10.1099/ijsem.0.000675. [DOI] [PubMed] [Google Scholar]
- 6.Esteves AI, Hardoim CC, Xavier JR, Gonçalves JM, Costa R. 2013. Molecular richness and biotechnological potential of bacteria cultured from Irciniidae sponges in the north-east Atlantic. FEMS Microbiol Ecol 85:519–536. doi: 10.1111/1574-6941.12140. [DOI] [PubMed] [Google Scholar]
- 7.Gonçalves AC, Franco T, Califano G, Dowd SE, Pohnert G, Costa R. 2015. Draft genome sequence of Vibrio sp. strain Vb278, an antagonistic bacterium isolated from the marine sponge Sarcotragus spinosulus. Genome Announc 3(3):e00521-15. doi: 10.1128/genomeA.00521-15. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Franco T, Califano G, Gonçalves AC, Cúcio C, Costa R. 2016. Draft genome sequence of Vibrio sp. strain Evh12, a bacterium retrieved from the gorgonian coral Eunicella verrucosa. Genome Announc 4:e01729-15. doi: 10.1128/genomeA.01729-15. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R. 2014. The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res 42:D206–D214. doi: 10.1093/nar/gkt1226. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Yu T, Zhang Z, Fan X, Shi X, Zhang X-H. 2014. Aquimarina megaterium sp. nov., isolated from seawater. Int J Syst Evol Microbiol 64:122–127. doi: 10.1099/ijs.0.055517-0. [DOI] [PubMed] [Google Scholar]
- 11.Xu T, Yu M, Lin H, Zhang Z, Liu J, Zhang X-H. 2015. Genomic insight into Aquimarina longa SW024T: its ultra-oligotrophic adapting mechanisms and biogeochemical functions. BMC Genomics 16:772. doi: 10.1186/s12864-015-2005-3. [DOI] [PMC free article] [PubMed] [Google Scholar]