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Recovery of Previously Uncultured Bacterial Genera from Three Mediterranean Sponges.

ABSTRACT: Sponges often harbour a dense and diverse microbial community. Presently, a large discrepancy exists between the cultivable bacterial fraction from sponges and the community in its natural environment. Here, we aimed to acquire additional insights into cultivability of (previously uncultured) bacteria from three sponge species, namely Aplysina aerophoba, Corticium candelabrum and Petrosia ficiformis, by studying bacterial growth on five media in the form of 60 communities scraped from plates without antibiotics, as well as in the form of individual isolates that were grown on these media supplemented with antibiotics. We applied (double-)barcoded 16S ribosomal RNA (rRNA) gene amplicon sequencing for species identification. We show that previously uncultured bacteria can be cultivated using conventional plating and that application of antibiotics in the media can serve to capture a greater bacterial diversity. Moreover, we present criteria to address an important caveat of the plate scraping method whereby bacteria may be detected that did not actually grow. Fourteen out of 27 cultivated novel taxa (<95% identity of the 16S rRNA gene amplicon to reported species) belong to Actinobacteria, which indicates the presence of a large untapped reservoir of bioactive compounds. Three Flavobacteriaceae spp. were isolated that potentially constitute two new genera and one new species.

SUBMITTER: Versluis D

PROVIDER: S-EPMC5599449 | biostudies-literature | 2017 Oct

REPOSITORIES: biostudies-literature

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Recovery of Previously Uncultured Bacterial Genera from Three Mediterranean Sponges.

Versluis Dennis D McPherson Kyle K van Passel Mark W J MWJ Smidt Hauke H Sipkema Detmer D

Marine biotechnology (New York, N.Y.) 20170710 5

Sponges often harbour a dense and diverse microbial community. Presently, a large discrepancy exists between the cultivable bacterial fraction from sponges and the community in its natural environment. Here, we aimed to acquire additional insights into cultivability of (previously uncultured) bacteria from three sponge species, namely Aplysina aerophoba, Corticium candelabrum and Petrosia ficiformis, by studying bacterial growth on five media in the form of 60 communities scraped from plates wit ...[more]

PMID: 28695385

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Project description:BackgroundThe seamounts Ses Olives (SO), Ausias March (AM) and Emile Baudot (EB) at the Mallorca Channel (Balearic Islands, western Mediterranean), are poorly explored areas containing rich and singular sponge communities. Previous works have shown a large heterogeneity of habitats, including rhodolith beds, rocky, gravel and sandy bottoms and steeped slopes. This diversity of habitats provides a great opportunity for improving the knowledge of the sponges from Mediterranean seamounts.MethodsSponges were collected during several surveys carried out by the Balearic Center of the Spanish Institute of Oceanography at the Mallorca Channel seamounts. Samples were obtained using a beam-trawl, rock dredge and remote operated vehicle. Additional samples were obtained from fishing grounds of the Balearic Islands continental shelf, using the sampling device GOC-73. Sponges were identified through the analysis of morphological and molecular characters.ResultsA total of 60 specimens were analyzed, from which we identified a total of 19 species. Three species and one genus are new to science: Foraminospongia balearica gen. nov. sp. nov., Foraminospongia minuta gen. nov. sp. nov. and Paratimea massutii sp. nov. Heteroxya cf. beauforti represents the first record of the genus Heteroxya in the Mediterranean Sea. Additionally, this is the second report of Axinella spatula and Haliclona (Soestella) fimbriata since their description. Moreover, the species Petrosia (Petrosia) raphida, Calyx cf. tufa and Lanuginella pupa are reported for the first time in the Mediterranean Sea. Petrosia (Strongylophora) vansoesti is reported here for the first time in the western Mediterranean Sea. Haliclona (S.) fimbriata is reported here for the first time in the north-western Mediterranean Sea. Hemiasterella elongata is reported here for the second time in the Mediterranean Sea. The species Melonanchora emphysema, Rhabdobaris implicata, Polymastia polytylota, Dragmatella aberrans, Phakellia ventilabrum and Pseudotrachya hystrix are reported for first time off Balearic Islands. Following the Sponge Barcoding project goals, we have sequenced the Cytochrome Oxidase subunit I (COI) and the 28S ribosomal fragment (C1-D2 domains) for Foraminospongia balearica sp. nov., Foraminospongia minuta sp. nov., H. cf. beauforti and C. cf. tufa, and the COI for Paratimea massuti sp. nov. We also provide a phylogenetic analysis to discern the systematic location of Foraminospongia gen. nov., which, in accordance to skeletal complement, is placed in the Hymerhabdiidae family. A brief biogeographical discussion is provided for all these species, with emphasis on the sponge singularity of SO, AM and the EB seamounts and the implications for their future protection.

Project description:Recent reviews have reinforced sponge-associated bacteria as a valuable source of structurally diverse secondary metabolites with potent biological properties, which makes these microbial communities promising sources of new drug candidates. However, the overall diversity of secondary metabolite biosynthetic potential present in bacteria is difficult to access due to the fact that the majority of bacteria are not readily cultured in the laboratory. Thus, use of cultivation-independent approaches may allow accessing "silent" and "cryptic" secondary metabolite biosynthetic gene clusters present in bacteria that cannot yet be cultured. In the present study, we investigated the diversity of secondary metabolite biosynthetic gene clusters (BGCs) in metagenomes of bacterial communities associated with three sponge species: Clathria reinwardti, Rhabdastrella globostellata, and Spheciospongia sp. The results reveal that the three metagenomes contain a high number of predicted BGCs, ranging from 282 to 463 BGCs per metagenome. The types of BGCs were diverse and represented 12 different cluster types. Clusters predicted to encode fatty acid synthases and polyketide synthases (PKS) were the most dominant BGC types, followed by clusters encoding synthesis of terpenes and bacteriocins. Based on BGC sequence similarity analysis, 363 gene cluster families (GCFs) were identified. Interestingly, no GCFs were assigned to pathways responsible for the production of known compounds, implying that the clusters detected might be responsible for production of several novel compounds. The KS gene sequences from PKS clusters were used to predict the taxonomic origin of the clusters involved. The KS sequences were related to 12 bacterial phyla with Actinobacteria, Proteobacteria, and Firmicutes as the most predominant. At the genus level, the KSs were most related to those found in the genera Mycolicibacterium, Mycobacterium, Burkholderia, and Streptomyces. Phylogenetic analysis of KS sequences resulted in detection of two known 'sponge-specific' BGCs, i.e., SupA and SwfA, as well as a new 'sponge-specific' cluster related to fatty acid synthesis in the phylum Candidatus Poribacteria and composed only by KS sequences of the three sponge-associated bacterial communities assessed here.

Dataset Information

Recovery of Previously Uncultured Bacterial Genera from Three Mediterranean Sponges.

Publications

Recovery of Previously Uncultured Bacterial Genera from Three Mediterranean Sponges.

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