Characterization of the bacterial community of the chemically defended Hawaiian sacoglossan Elysia rufescens

Applied and Environmental Microbiology

Volumn 79, Issue 22, 2013, Pages 7073-7081

  Davis, Jeanette ^a   Fricke, W Florian ^b   Hamann, Mark T ^c   Esquenazi, Eduardo ^d,e   Dorrestein, Pieter C ^d,e   Hill, Russell T ^a  

^a UNIVERSITY OF MARYLAND CENTER FOR ENVIRONMENTAL SCIENCE   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MISSISSIPPI   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

454-PYROSEQUENCING; ANTICANCER PROPERTIES; BACTERIAL ASSEMBLAGES; BACTERIAL COMMUNITY; BACTERIAL DIVERSITY; EPIFLUORESCENCE MICROSCOPY; LONGITUDINAL SECTION; MATRIX-ASSISTED LASER;

BACTERIA; FLUORINE; MASS SPECTROMETRY; MOLECULES;

BODY FLUIDS;

ANTIMICROBIAL ACTIVITY; BACTERIUM; CHEMICAL DEFENSE; CHLOROPLAST; COMMUNITY STRUCTURE; MICROBIAL COMMUNITY; MOLECULAR ANALYSIS; SPECIES DIVERSITY;

HAWAIIAN ISLANDS;

BACTERIAL DNA; RNA 16S;

ANIMAL; ARTICLE; BIODIVERSITY; CLASSIFICATION; DNA SEQUENCE; GASTROPOD; GENETICS; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; MICROBIOLOGY; MYCOPLASMA; PHYLOGENY; VIBRIO;

ANIMALS; BIODIVERSITY; DNA, BACTERIAL; GASTROPODA; MYCOPLASMA; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; VIBRIO;

EID: 84886712356     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01568-13     Document Type: Article

References (77)

1. Benkendorff K. 2010. Molluscan biological and chemical diversity: secondary metabolites and medicinal resources produced by marine molluscs. Biol. Rev. Camb. Philos. Soc. 85:757-775.
2. De Bary HA. 1879. Die erscheinung der symbiose. Privately printed, Strasbourg.
3. Taylor MW, Radax R, Steger D, Wagner M. 2007. Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol. Mol. Biol. Rev. 71:295-347.
4. Holmström C, Kjelleberg S. 1994. The effect of external biological factors on settlement of marine invertebrate and new antifouling technology. Biofouling 8:147-160.
5. Donachie SP, Zdanowski MK. 1998. Potential digestive function of bacteria in krill Euphausia superba stomach. Aquat. Microb. Ecol. 14:129-136.
6. Mearns-Spragg A, Bregu A, Boyd KG, Burgess JG. 1998. Cross-species induction and enhancement of antimicrobial activity produced by epibiotic bacteria from marine algae and invertebrates, after exposure to terrestrial bacteria. Lett. Appl. Microbiol. 27:142-146.
7. Hill RT. 2004. Microbes from marine sponges: a treasure trove of biodiversity for natural products discovery, p 177-190. In Bull AT (ed), Microbial diversity and bioprospecting. ASM Press, Washington, DC.
8. Schmidt EW, Nelson JT, Rasko Sudek DAS, Eisen JA, Haygood MG, Ravel J. 2005. 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. 102:7315-7320.
9. Piel J, Hui D, Wen G, Butzke D, Platzer M, Fusetani N, Matsunaga S. 2004. Antitumor polyketide biosynthesis by an uncultivated bacterialsymbiont of the marine sponge Theonella swinhoei. Proc. Natl. Acad. Sci. U. S. A. 101:16222-16227.
10. Davidson SK, Allen SW, Lim GE, Anderson CM, Haygood MG. 2001. Evidence for the biosynthesis of bryostatins by the bacterial symbiont "Candidatus Endobugula sertula" of the bryozoan Bugula neritina. Appl. Environ. Microbiol. 67:4531-4537.
11. Proksch P, Edrada RA, Ebel R. 2002. Drugs from the sea-current status and microbiological implications. Appl. Microbiol. Biotechnol. 59:25-34.
12. Piel J. 2004. Metabolites from symbiotic bacteria. Nat. Prod. Rep. 21:519- 538.
13. Suarez-Jimenez GM, Burgos-Hernandez A, Ezquerra-Brauer JM. 2012. Bioactive peptides and depsipeptides with anticancer potential: sources from marine animals. Mar. Drugs 10:963-986.
14. Fisher CR. 1990. Chemoautotrophic and methanotrophic symbiosis in marine invertebrates. Rev. Aquat. Sci. 2:399-436.
15. Cavanaugh CM, McKiness ZP, Newton ILG, Stewart FJ. 2006. Marine chemosynthetic symbiosis, p 475-507. In Dworkin M, Falkow S, Rosenberg E, Schleifer K, Stackebrandt E (ed), The prokaryotes, 3rd ed, vol 1. Springer, New York, NY.
16. Dubilier N, Bergin C, Lott C. 2008. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat. Rev. Microbiol. 6:725-740.
17. Taylor JD, Glover EA. 2010. Chemosymbiotic bivalves, p 107-135. In Kiel S (ed), The vent and seep biota: aspects from microbes to ecosystems, vol. 33. Topics in Geobiology. Springer, Dordrecht, Netherlands.
18. Urakawa H, Dubilier N, Fujiwara Y, Cunningham DE, Kojima S, Stahl DA. 2005. Hydrothermal vent gastropods from the same family (Provannidae) harbour e- and γ-proteobacterial endosymbionts. Environ. Microbiol. 7:750-754.
19. Azam F. 1998. Microbial control of oceanic carbon flux: the plot thickens. Science 280:694-696.
20. Sminia T, Van der Knaap WPW. 1986. Immunorecognition in invertebrates with special reference to mollusks, p 112-124. In Brehelin M (ed), Immunity in invertebrates. Springer-Verlag, Berlin, Germany.
21. Hooper C, Day R, Slocombe R, Handlinger J, Benkendorff K. 2007. Stress and immune responses in abalone: limitations in current knowledge and investigative methods based on other models. Fish Shellfish Immunol. 22:363-379.
22. Cimino G, Passeggio A, Sodano G, Spinella A, Villani G. 1991. Alarm pheromones from the Mediterranean opisthobranch Haminoea navicula. Experientia 47:61-63.
23. Zatylny C, Gagnon J, Boucaud-Camou E, Henry J. 2000. ILME: a waterbourne pheromonal peptide released by the eggs of Sepia officinalis. Biochem. Biophys. Res. Commun. 275:217-222.
24. Cummins SF, Nichols AE, Schein CH, Nagle GT. 2006. Newly identified water-borne protein pheromones interact with attractin to stimulate mate attraction in Aplysia. Peptides 27:597-606.
25. Craig AG. 2000. The characterization of conotoxins. J. Toxicol. Toxin Rev. 19:53-93.
26. Kanda A, Iwakoshi-Ukena E, Takuwa-Kuroda K, Minakata H. 2003. Isolation and characterization of novel tachykinins from the posterior salivary gland of the common octopus Octupus vulgaris. Peptides 24:35- 43.
27. Pawlik JR, Albizati KF, Faulkner DJ. 1986. Evidence of a defensive role for limatulone, a novel triterpene from the interdial limpet Collisella limatula. Mar. Ecol. Prog. Ser. 30:251-260.
28. Marin A, Alvarez LA, Cimino G, Spinella A. 1991. Chemical defense in cephalaspidean gastropods: origin, anatomical location and ecological roles. J. Molluscan Stud. 65:121-131.
29. Kelley WP, Wolters AM, Sack JT, Jockusch RA, Jurchen JC, Williams ER, Sweedler JV, Gilly WF. 2003. Characterization of a novel gastropod toxin (6-bromo-2-mercaptotryptamine) that inhibits shaker K channel activity. J. Biol. Chem. 278:34934-34942.
30. Derby CD, Kicklighter CE, Johnson PM, Zang X. 2007. Chemical composition of inks of diverse marine molluscs suggests convergent chemical defenses. J. Chem. Ecol. 33:1105-1113.
31. Carmona L, Malaquias MAE, Gosliner TM, Pola M, Cervera JL. 2011. Amphi-atlantic distributions and cryptic species in sacoglossan sea slugs. J. Molluscan Stud. 77:401-412.
32. Wägele H. 2004. Potential key characters in opisthobranchia (Gastropoda, Mollusca) enhancing adaptive radiation. Org. Div. Evol. 4:175- 188.
33. Rumpho ME, Summer EJ, Green BJ, Fox TC, Manhart JR. 2001. Mollusc/algal chloroplast symbiosis: how can isolated chloroplasts con-tinue to function for months in the cytosol of a sea slug in the absence of an algal nucleus? Zoology 104:303-312.
34. Pelletreau KN, Bhattacharya D, Price DC, Worful JM, Moustafa A, Rumpho ME. 2011. Sea slug kleptoplasty and plastid maintenance in a metazoan. Plant Physiol. 155:1561-1565.
35. Rumpho ME, Summer EJ, Manhart JR. 2000. Solar-powered sea slugs. Mollusc/algal chloroplast symbiosis. Plant Physiol. 123:29-38.
36. Pierce SK, Fang X, Schwartz JA, Jiang X, Zhao W, Curthis NE, Kocot KM, Yang B, Wang J. 2012. Transcriptomic evidence for the expression of horizontally transferred algal nuclear genes in the photosynthetic sea slug, Elysia chlorotica. Mol. Biol. Evol. 29:1545-1556.
37. Bhattacharya D, Pelletreau KN, Price DC, Sarver KE, Rumpho ME. 2013. Genome analysis of Elysia chlorotica egg DNA provides no evidence for horizontal gene transfer into the germ line of this kleptoplastic mollusc. Mol. Biol. Evol. 30:1843-1852.
38. Avila C. 1995. Natural products of opisthobranch molluscs: a biological review. Oceanogr. Mar. Biol. Annu. Rev. 33:487-559.
39. Smyrniotopoulos V, Abatis D, Tziveleka LA, Tsitsimpikou C, Roussis V, Loukis A, Vagias C. 2003. Acetylene sesquiterpenoid esters from the green alga Caulerpa prolifera. J. Nat. Prod. 66:21-24.
40. Dobretsov S, Dahms HU, Harder T, Qian PY. 2006. Allelochemical defense against epibiosis in the macroalga Caulerpa racemosa var. turbinata. Mar. Ecol. Prog. Ser. 318:165-175.
41. Marin A, Ros J. 2004. Chemical defenses in sacoglossan opisthobranchs: taxonomic trends and evolutive implications. Sci. Mar. 68:227-241.
42. Devine SP, Pelletreau KN, Rumpho ME. 2012. 16S rDNA-based metagenomic analysis of bacterial diversity associated with two populations of the kleptoplastic sea slug Elysia chlorotica and its algal prey Vaucheria litorea. Biol. Bull. 223:138-154.
43. Becerro MA, Goetz G, Paul VJ, Scheuer PJ. 2001. Chemical defenses of the sacoglossan mollusk Elysia rufescens and its host alga Bryopsis sp. J. Chem. Ecol. 27:2287-2299.
44. Hamann MT, Scheuer PJ. 1993. Kahalalide F: a bioactive depsipeptide from the sacoglossan mollusk Elysia rufescens and the green alga Bryopsis sp. J. Am. Chem. Soc. 115:5825-5826.
45. Hamann MT, Otto CS, Scheuer PJ. 1996. Kahalalides: bioactive peptides from a marine mollusk Elysia rufescens and its algal diet Bryopsis sp. J. Org. Chem. 61:6594-6600.
46. Hamann MT. 2004. Technology evaluation: Kahalalide F, PharmaMar. Curr. Opin. Mol. Ther. 6:657-665.
47. Gao J, Hamann MT. 2011. Chemistry and biology of kahalalides. Chem. Rev. 111:3208-3235.
48. Hill RT, Enticknap J, Rao KV, Hamann MT. August 2007. Kahalalideproducing bacteria. US patent 20070196901.
49. Montalvo NF, Mohamed NM, Entichnap JJ, Hill RT. 2005. Novel actinobacteria from marine sponges. Antonie Van Leeuwenhoek 87: 29 -36.
50. Lane DJ. 1991. 16S/23S rRNA sequencing, p 115-175. In Stackebrandt E, GoodfellowM(ed), Nucleic acid techniques in bacterial systematics. John Wiley and Sons, New York, NY.
51. Somerville CC, Knight IT, Straube WL, Colwell RR. 1989. Simple, rapid method for direct isolation of nucleic acids from aquatic environments. Appl. Environ. Microbiol. 55:548-554.
52. Muyzer G, DeWaal EC, Uitterlinden AG. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59:695-700.
53. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335-336.
54. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541.
55. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
56. Huse SM, Welch DM, Morrison HG, Sogin ML. 2010. Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ. Microbiol. 12:1889-1898.
57. Yue JC, Clayton MK. 2005. A similarity measure based on species proportions. Commun. Stat. Theory Methods 34:2123-2131.
58. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar Buchner A, Lai T, Steppi S, Jobb G, Förster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, König A, Liss T, Lüssmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371.
59. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
60. Simmons TL, Coates RC, Clark BR, Engene N, Gonzalez D, Esquenazi E, Dorrestein PC, Gerwick WH. 2008. Biosynthetic origin of natural products isolated from marine microorganisms-invertebrate assemblages. Proc. Natl. Acad. Sci. U. S. A. 105:4587-4594.
61. Ruby EG. 1996. Lessons from a cooperative, bacterial-animal association. The Vibrio fischeri-Euprymna scolopes light organ symbiosis. Annu. Rev. Microbiol. 50:591-624.
62. Faruque SM, Albert MJ, Mekalanos JJ. 1998. Epidemiology, genetics, and ecology of toxigenic Vibrio cholera. Microbiol. Mol. Biol. Rev. 62: 1301-1314.
63. Wietz M, Mansson M, Gotfredsen CH, Larsen TO, Gram L. 2010. Antibacterial compounds from marine Vibrionaceae isolated on a global expedition. Mar. Drugs 8:2946-2960.
64. Mansson M, Gram L, Larsen TO. 2011. Production of bioactive secondary metabolites by marine Vibrionaceae. Mar. Drugs 9:1440-1468.
65. Whithear K. 2001. Diseases due to mycoplasmas, p 413-422. In Williams ES, Barker IK (ed), Infectious diseases of wild mammals. Iowa University Press, Ames, IA.
66. Fraune S, Zimmer M. 2008. Host-specificity of environmentally transmitted Mycoplasma-like isopod symbionts. Environ. Microbiol. 10:2497- 2504.
67. Bano N, DeRae SA, Bennett W, Vasquez L, Hollibaugh JT. 2007. Dominance of Mycoplasma in the guts of the Long-Jawed Mudsucker, Gillichthys mirabilis, from five California salt marshes. Environ. Microbiol. 9:2636-2641.
68. Huang ZB, Guo F, Zhao J, Li WD, Ke CH. 2010. Molecular analysis of the intestinal bacterial flora in cage-cultured adult small abalone, Haliotis diversicolor. Aquac. Res. 41:760-769.
69. Naidoo K, Maneveldt G, Ruck K, Bolton J. 2006. A comparison of various seaweed-based diets and formulated feed growth rate of abalone in a land-based aquaculture system. J. Appl. Phycol. 18:437-443.
70. Erasmus JH, Cook PA, Coyne VE. 1997. The role of bacteria in the digestion of seaweed by the abalone Haliotis midae. Aquaculture 155:377- 386.
71. Hollants J, Leroux O, Leliaert F, Decleyre H, De Clerck O, Willems A. 2011. Who is in there? Exploration of endophytic bacteria within the siphonous green seaweed Bryopsis (Bryopsidales, Chlorophyta). PLoS One 6:e26458. doi:10.1371/journal.pone.0026458.
72. Hollants J, Decleyre H, Leliaert F, De Clerck O, Willems A. 2011. Life without cell membrane: challenging the specificity of bacterial endophytes within Bryopsis (Bryopsidales, Chlorophyta). BMC Microbiol. 11:255- 265.
73. Nyholm SV, Stabb EV, Ruby EG, McFall-Ngai MJ. 2000. Establishment of an animal-bacterial association: recruiting symbiotic vibrios from the environment. Proc. Natl. Acad. Sci. U. S. A. 97:10231-10235.
74. Nyholm SV, Deplancke B, Gaskins HR, Apicella MA, McFall-Ngai MJ. 2002. Roles of Vibrio fischeri and nonsymbiotic bacteria in the dynamics of mucus secretion during symbiont colonization of the Euprymna scolopes light organ. Appl. Environ. Microbiol. 68:5113-5122.
75. Trench RK. 1975. Of leaves that crawl: functional chloroplast in animal cells. Symp. Soc. Exp. Biol. 29:229-265.
76. Paul VJ, Van Alstyne KL. 1988. Use of ingested algal diterpenoid by Elysia halimedae Macnae (Opisthobranchia: Ascoglossa) as antipredator defenses. J. Exp. Mar. Biol. Ecol. 119:15-29.
77. Rumpho, ME, Mujer CV, Andrews DL, Manhart JR, Pierce SK. 1994. Extraction of DNA from mucilaginous tissues of a sea slug (Elysia chlorotica). Biotech. 17:1097-1101.