Microhabitats Within Venomous Cone Snails Contain Diverse Actinobacteria

Overview

Journal Appl Environ Microbiol

Specialties Environmental Health
Microbiology

Date 2009 Sep 15

PMID 19749071

Citations 26

Authors

Olivier Peraud

Jason S Biggs

Ronald W Hughen

Alan R Light

Gisela P Concepcion

Baldomero M Olivera

Eric W Schmidt

Affiliations

Soon will be listed here.

Abstract

Actinomycetes can be symbionts in diverse organisms, including both plants and animals. Some actinomycetes benefit their host by producing small molecule secondary metabolites; the resulting symbioses are often developmentally complex. Actinomycetes associated with three cone snails were studied. Cone snails are venomous tropical marine gastropods which have been extensively examined because of their production of peptide-based neurological toxins, but no microbiological studies have been reported on these organisms. A microhabitat approach was used in which dissected tissue from each snail was treated as an individual sample in order to explore bacteria in the tissues separately. Our results revealed a diverse, novel, and highly culturable cone snail-associated actinomycete community, with some isolates showing promising bioactivity in a neurological assay. This suggests that cone snails may represent an underexplored reservoir of novel actinomycetes of potential interest for drug discovery.

Citing Articles

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References

Volksch B, Ullrich M, Fritsche W . Identification and population dynamics of bacteria in leaf spots of soybean. Microb Ecol. 2013; 24(3):305-11. DOI: 10.1007/BF00167788. View

Mueller U, Dash D, Rabeling C, Rodrigues A . Coevolution between attine ants and actinomycete bacteria: a reevaluation. Evolution. 2008; 62(11):2894-912. DOI: 10.1111/j.1558-5646.2008.00501.x. View

Reysenbach A, Giver L, Wickham G, Pace N . Differential amplification of rRNA genes by polymerase chain reaction. Appl Environ Microbiol. 1992; 58(10):3417-8. PMC: 183115. DOI: 10.1128/aem.58.10.3417-3418.1992. View

Weisburg W, Barns S, Pelletier D, Lane D . 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol. 1991; 173(2):697-703. PMC: 207061. DOI: 10.1128/jb.173.2.697-703.1991. View

Roller C, Wagner M, Amann R, Ludwig W, Schleifer K . In situ probing of gram-positive bacteria with high DNA G + C content using 23S rRNA-targeted oligonucleotides. Microbiology (Reading). 1994; 140 ( Pt 10):2849-58. DOI: 10.1099/00221287-140-10-2849. View

Saitou N, Nei M . The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987; 4(4):406-25. DOI: 10.1093/oxfordjournals.molbev.a040454. View

Schmidt E, Nelson J, Rasko D, Sudek S, Eisen J, Haygood M . Patellamide A and C biosynthesis by a microcin-like pathway in Prochloron didemni, the cyanobacterial symbiont of Lissoclinum patella. Proc Natl Acad Sci U S A. 2005; 102(20):7315-20. PMC: 1091749. DOI: 10.1073/pnas.0501424102. View

Espiritu D, Watkins M, Cartier G, Cruz L, Olivera B . Venomous cone snails: molecular phylogeny and the generation of toxin diversity. Toxicon. 2001; 39(12):1899-916. DOI: 10.1016/s0041-0101(01)00175-1. View

Light A, Hughen R, Zhang J, Rainier J, Liu Z, Lee J . Dorsal root ganglion neurons innervating skeletal muscle respond to physiological combinations of protons, ATP, and lactate mediated by ASIC, P2X, and TRPV1. J Neurophysiol. 2008; 100(3):1184-201. PMC: 6195653. DOI: 10.1152/jn.01344.2007. View

10.

Zhang H, Zhang W, Jin Y, Jin M, Yu X . A comparative study on the phylogenetic diversity of culturable actinobacteria isolated from five marine sponge species. Antonie Van Leeuwenhoek. 2007; 93(3):241-8. DOI: 10.1007/s10482-007-9196-9. View

11.

Martin D, McClelland D, Herd M, Sutton K, Hall M, Lee K . Gabapentin-mediated inhibition of voltage-activated Ca2+ channel currents in cultured sensory neurones is dependent on culture conditions and channel subunit expression. Neuropharmacology. 2002; 42(3):353-66. DOI: 10.1016/s0028-3908(01)00181-2. View

12.

De Rosa S, Milone A, Kujumgiev A, Stefanov K, Nechev I, Popov S . Metabolites from a marine bacterium Pseudomonas/Alteromonas, associated with the sponge Dysidea fragilis. Comp Biochem Physiol B Biochem Mol Biol. 2000; 126(3):391-6. DOI: 10.1016/s0305-0491(00)00208-x. View

13.

Olivera B, Quik M, Vincler M, McIntosh J . Subtype-selective conopeptides targeted to nicotinic receptors: Concerted discovery and biomedical applications. Channels (Austin). 2008; 2(2):143-52. DOI: 10.4161/chan.2.2.6276. View

14.

Webster N, Wilson K, Blackall L, Hill R . Phylogenetic diversity of bacteria associated with the marine sponge Rhopaloeides odorabile. Appl Environ Microbiol. 2001; 67(1):434-44. PMC: 92596. DOI: 10.1128/AEM.67.1.434-444.2001. View

15.

Lozupone C, Hamady M, Knight R . UniFrac--an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics. 2006; 7:371. PMC: 1564154. DOI: 10.1186/1471-2105-7-371. View

16.

Kaltenpoth M, Gottler W, Herzner G, Strohm E . Symbiotic bacteria protect wasp larvae from fungal infestation. Curr Biol. 2005; 15(5):475-9. DOI: 10.1016/j.cub.2004.12.084. View

17.

Heuer H, Krsek M, Baker P, Smalla K, Wellington E . Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol. 1997; 63(8):3233-41. PMC: 168621. DOI: 10.1128/aem.63.8.3233-3241.1997. View

18.

Sudek S, Lopanik N, Waggoner L, Hildebrand M, Anderson C, Liu H . Identification of the putative bryostatin polyketide synthase gene cluster from "Candidatus Endobugula sertula", the uncultivated microbial symbiont of the marine bryozoan Bugula neritina. J Nat Prod. 2007; 70(1):67-74. DOI: 10.1021/np060361d. View

19.

Xin Y, Huang J, Deng M, Zhang W . Culture-independent nested PCR method reveals high diversity of actinobacteria associated with the marine sponges Hymeniacidon perleve and Sponge sp. Antonie Van Leeuwenhoek. 2008; 94(4):533-42. DOI: 10.1007/s10482-008-9270-y. View

20.

Haeder S, Wirth R, Herz H, Spiteller D . Candicidin-producing Streptomyces support leaf-cutting ants to protect their fungus garden against the pathogenic fungus Escovopsis. Proc Natl Acad Sci U S A. 2009; 106(12):4742-6. PMC: 2660719. DOI: 10.1073/pnas.0812082106. View