Host differentially expressed genes during association with its defensive endosymbiont

Biological Bulletin

Volumn 226, Issue 2, 2014, Pages 152-163

  Mathew, Meril ^a   Lopanik, Nicole B ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOFILM; BRYOZOAN; COLONY; ENDOSYMBIONT; GENE EXPRESSION; HOST; HOST-SYMBIONT INTERACTION; LIFE HISTORY TRAIT; MUTUALISM; REPRODUCTIVE BIOLOGY;

ACTIN; BRYOSTATIN;

ANIMAL; ARTICLE; BRYOZOA; DRUG EFFECT; GAMMAPROTEOBACTERIA; GENE EXPRESSION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; POLYMERASE CHAIN REACTION; SYMBIOSIS;

ACTINS; ANIMALS; BASE SEQUENCE; BRYOSTATINS; BRYOZOA; GAMMAPROTEOBACTERIA; GENE EXPRESSION; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; SYMBIOSIS;

EID: 84899914864     PISSN: 00063185     EISSN: None     Source Type: Journal    
DOI: 10.1086/BBLv226n2p152     Document Type: Article

References (84)

1. Akita, Y. 2008. Protein kinase C: multiple roles in the function of, and signaling mediated by, the cytoskeleton. FEBS J. 275: 3995-4004.
2. Aktories, K., and J. T. Barbieri. 2005. Bacterial cytotoxins: targeting eukaryotic switches. Nat. Rev. Microbiol. 3: 397-410.
3. Balasubramanian, N., G. Nascimento, R. Ferreira, M. Martinez, and N. Simoes. 2012. Pepsin-like aspartic protease (Sc-ASP155) cloning, molecular characterization and gene expression analysis in developmental stages of nematode Steinernema carpocapsae. Gene 500: 164-171.
4. Banta, W. C. 1969. The body wall of cheilostome Bryozoa. II. Interzoidal communication organs. J. Morphol. 129: 149-169.
5. Barr, P. M., H. M. Lazarus, B. W. Cooper, M. D. Schluchter, A. Panneerselvam, J. W. Jacobberger, J. W. Hsu, N. Janakiraman, A. Simic, A. Dowlati, and S. C. Remick. 2009. Phase II study of bryostatin 1 and vincristine for aggressive non-Hodgkin lymphoma relapsing after an autologous stem cell transplant. Am. J. Hematol. 84: 484-487.
6. Bobin, G. 1977. Interzooecial communications and the funicular system. Pp. 307-333 in Biology of Bryozoans, R. M. Woollacott and R. L. Zimmer, eds. Academic Press, New York.
7. Carle, K. J., and E. Ruppert. 1983. Comparative ultrastructure of the bryozoan funiculus: a blood vessel homologue. J. Zoolog. Syst. Evol. Res. 21: 181-193.
8. Carlton, J., and J. Hodder. 1995. Biogeography and dispersal of coastal marine organisms: experimental studies on a replica of a 16th-century sailing vessel. Mar. Biol. 121: 721-730.
9. Chaston, J., and H. Goodrich-Blair. 2010. Common trends in mutualism revealed by model associations between invertebrates and bacteria. FEMS Microbiol. Rev. 34: 41-58.
10. Clamp, A., and G. C. Jayson. 2002. The clinical development of the bryostatins. Anticancer Drugs 13: 673-683.
11. Davidson, S. K. 1999. Biology of the bryostatins in the marine bryozoan Bugula neritina: symbiosis, cryptic speciation and chemical defense. Ph.D. dissertation, University of California San Diego, La Jolla.
12. Davidson, S. K., S. W. Allen, G. E. Lim, C. M. Anderson, and M. G. Haygood. 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.
13. Davison, A., and M. Blaxter. 2005. Ancient origin of glycosyl hydrolase family 9 cellulase genes. Mol. Biol. Evol. 22: 1273-1284
14. De Vries, D. J., C. L. Herald, G. R. Pettit, and P. M. Blumberg. 1988. Demonstration of sub-nanomolar affinity of bryostatin 1 for the phorbol ester receptor in rat brain. Biochem. Pharmacol. 37: 4069-4073.
15. Deinema, M. H., and L. Zevenhuizen. 1971. Formation of cellulose fibrils by gram-negative bacteria and their role in bacterial flocculation. Arch. Microbiol. 78: 42-57.
16. Diatchenko, L., Y. Lau, A. P. Campbell, A. Chenchik, F. Moqadam, B. Huang, S. Lukyanov, K. Lukyanov, N. Gurskaya, and E. D. Sverdlov. 1996. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc. Natl. Acad. Sci. USA 93: 6025-6030.
17. Esseling, J. J., F. G. P. Lhuissier, and A. M. C. Emons. 2003. Nod factor-induced root hair curling: continuous polar growth towards the point of nod factor application. Plant Physiol. 132: 1982-1988
18. Etcheberrigaray, R., M. Tan, I. Dewachter, C. Kuiperi, I. Van der Auwera, S. Wera, L. X. Qiao, B. Bank, T. J. Nelson, A. P. Kozikowski, F. Van Leuven, and D. L. Alkon. 2004. Therapeutic effects of PKC activators in Alzheimer's disease transgenic mice. Proc. Natl. Acad. Sci. USA 101: 11141-11146.
19. Ferree, P. M., H. M. Frydman, J. M. Li, J. Cao, E. Wieschaus, and W. Sullivan. 2005. Wolbachia utilizes host microtubules and Dynein for anterior localization in the Drosophila oocyte. PLoS Pathog. 1: e14
20. Franzenburg, S., J. Walter, S. Kunzel, J. Wang, J. F. Baines, T. C. G. Bosch, and S. Fraune. 2013. Distinct antimicrobial peptide expression determines host species-specific bacterial associations. Proc. Natl. Acad. Sci. USA 110: E3730-E3738.
21. Gordon, D. P. 1974. Ultrastructure of communication pore areas in two bryozoans. Doc. Lab. Geol. Fac. Sci. Lyon 3: 187-192.
22. Gordon, D. P., and S. F. Mawatari. 1992. Atlas of marine-fouling Bryozoa of New Zealand ports and harbours. Misc. Publ. NZ Oceanogr. Inst. 107: 1-52.
23. Haine, E. R. 2008. Symbiont-mediated protection. Proc. R. Soc. B Biol. Sci. 275: 353-361.
24. Hart, M. J., Y. Maru, D. Leonard, O. N. Witte, T. Evans, and R. A. Cerione. 1992. A GDP dissociation inhibitor that serves as a GTPase inhibitor for the Ras-like protein CDC42Hs. Science 258: 812-815
25. Haygood, M. G., and S. K. Davidson. 1997. Small-subunit rRNA genes and in situ hybridization with oligonucleotides specific for the bacterial symbionts in the larvae of the bryozoan Bugula neritina and proposal of "Candidatus endobugula sertula." Appl. Environ. Microbiol. 63: 4612-4616.
26. Haygood, M. G., E. W. Schmidt, S. K. Davidson, and D. J. Faulkner. 1999. Microbial symbionts of marine invertebrates: opportunities for microbial biotechnology. J. Mol. Microbiol. Biotechnol. 1: 33-43
27. Henrissat, B. 1991. A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 280: 309-316
28. Ibrahim, A. M. A., and Y. Kim. 2008. Transient expression of protein tyrosine phosphatases encoded in Cotesia plutellae bracovirus inhibits insect cellular immune responses. Naturwissenschaften 95: 25-32
29. Itoh, Y., X. Wang, B. J. Hinnebusch, J. F. Preston III, and T. Romeo. 2005. Depolymerization of-1,6-N-acetyl-D-glucosamine disrupts the integrity of diverse bacterial biofilms. J. Bacteriol. 187: 382-387
30. Jackson, J. 1977. Competition on marine hard substrata: the adaptive significance of solitary and colonial strategies. Am. Nat. 111: 743-767
31. Kaplan, J. B., C. Ragunath, N. Ramasubbu, and D. H. Fine. 2003. Detachment of Actinobacillus actinomycetemcomitans biofilm cells by an endogenous-hexosaminidase activity. J. Bacteriol. 185: 4693-4698.
32. Kaplan, J. B., C. Ragunath, K. Velliyagounder, D. H. Fine, and N. Ramasubbu. 2004a. Enzymatic detachment of Staphylococcus epidermidis biofilms. Antimicrob. Agents Chemother. 48: 2633-2636
33. Kaplan, J. B., K. Velliyagounder, C. Ragunath, H. Rohde, D. Mack, J. K. M. Knobloch, and N. Ramasubbu. 2004b. Genes involved in the synthesis and degradation of matrix polysaccharide in Actinobacillus actinomycetemcomitans and Actinobacillus pleuropneumoniae biofilms. J. Bacteriol. 186: 8213-8220.
34. Kellner, R. L. L. 1999. What is the basis of pederin polymorphism in Paederus riparius rove beetles? The endosymbiotic hypothesis. Entomol. Exp. Appl. 93: 41-49.
35. Kellner, R. L. L. 2001. Suppression of pederin biosynthesis through antibiotic elimination of endosymbionts in Paederus sabaeus. J. Insect Physiol. 47: 475-483.
36. Kellner, R. L. L. 2002. Molecular identification of an endosymbiotic bacterium associated with pederin biosynthesis in Paederus sabaeus (Coleoptera: Staphylinidae). Insect Biochem. Mol. Biol. 32: 389-395
37. Kellner, R. L. L., and K. Dettner. 1996. Differential efficacy of toxic pederin in deterring potential arthropod predators of Paederus (Coleoptera: Staphylinidae) offspring. Oecologia 107: 293-300.
38. Keough, M. J. 1989a. Dispersal of the bryozoan Bugula neritina and effects of adults on newly metamorphosed juveniles. Mar. Ecol. Prog. Ser. 57: 163-172.
39. Keough, M. J. 1989b. Variation in growth rate and reproduction of the bryozoan Bugula neritina. Biol. Bull. 177: 277-286.
40. Kim, J., R. Hepat, D. Lee, and Y. Kim. 2013. Protein tyrosine phosphatase encoded in Cotesia plutellae bracovirus suppresses a larva-to-pupa metamorphosis of the diamondback moth, Plutella xylostella. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 166: 60-69
41. Kimbell, J. R., and M. J. McFall-Ngai. 2004. Symbiont-induced changes in host actin during the onset of a beneficial animal-bacterial association. Appl. Environ. Microbiol. 70: 1434-1441.
42. Kraft, A. S., J. B. Smith, and R. L. Berkow. 1986. Bryostatin, an activator of the calcium phospholipid-dependent protein kinase, blocks phorbol ester-induced differentiation of human promyelocytic leukemia cells HL-60. Proc. Natl. Acad. Sci. USA 83: 1334-1338.
43. Lestari, P., K. Van, M. Y. Kim, C. H. Hwang, B.-W. Lee, and S.-H. Lee. 2006. Differentially expressed genes related to symbiotic association in a supernodulating soybean mutant and its wild-type. Mol. Plant Pathol. 7: 235-247.
44. Lindquist, N. 1996. Palatability of invertebrate larvae to corals and sea anemones. Mar. Biol. 126: 745-755.
45. Lindquist, N. 2002. Chemical defense of early life stages of benthic marine invertebrates. J. Chem. Ecol. 28: 1987-2000.
46. Lindquist, N., and M. E. Hay. 1996. Palatability and chemical defense of marine invertebrate larvae. Ecol. Monogr. 66: 431-450.
47. Lo, N., H. Watanabe, and M. Sugimura. 2003. Evidence for the presence of a cellulase gene in the last common ancestor of bilaterian animals. Proc. R. Soc. Lond. B Biol. Sci. 270: S69-S72.
48. Login, F. H., S. Balmand, A. Vallier, C. Vincent-Monegat, A. Vigneron, M. Weiss-Gayet, D. Rochat, and A. Heddi. 2011. Antimicrobial peptides keep insect endosymbionts under control. Science 334: 362-365.
49. Lopanik, N. B. 2014. Chemical defensive symbiosis in the marine environment. Funct. Ecol. 28: 328-340.
50. Lopanik, N., N. Lindquist, and N. Targett. 2004. Potent cytotoxins produced by a microbial symbiont protect host larvae from predation. Oecologia 139: 131-139.
51. Lopanik, N. B., N. M. Targett, and N. Lindquist. 2006. Ontogeny of a symbiont-produced chemical defense in Bugula neritina (Bryozoa). Mar. Ecol. Prog. Ser. 327: 183-191.
52. Lutaud, G. 1991. The organization of the mesenchymal tissues in a cheilostomate zooecium. Pp. 219-228 in Bryozoa Living and Fossil, F. P. Bigey, ed. Bulletin de la Societe des Sciences Naturelles de l'Ouest de la France. Memoire Hors Serie, France.
53. Mandel, M. J., M. S. Wollenberg, E. V. Stabb, K. L. Visick, and E. G. Ruby. 2009. A single regulatory gene is sufficient to alter bacterial host range. Nature 458: 215-218.
54. McFall-Ngai, M., M. G. Hadfield, T. C. G. Bosch, H. V. Carey, T. Domazet-Loso, A. E. Douglas, N. Dubilier, G. Eberl, T. Fukami, S. F. Gilbert, et al. 2013. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl. Acad. Sci. USA 110: 3229-3236.
55. Moran, N. A. 2006. Symbiosis. Curr. Biol. 16: R866-R871
56. Oliver, K. M., J. A. Russell, N. A. Moran, and M. S. Hunter. 2003. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Natl. Acad. Sci. USA 100: 1803-1807.
57. Oliver, K. M., N. A. Moran, and M. S. Hunter. 2005. Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc. Natl. Acad. Sci. USA 102: 12795-12800.
58. Ostrovsky, A. N. 1998. Comparative studies of ovicell anatomy and reproductive patterns in Cribrilina annulata and Celleporella hyaline (Bryozoa: Cheilostomatida). Acta Zool. (Stockh.) 79: 287-318
59. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29: e45.
60. Pfaffl, M. W., G. W. Horgan, and L. Dempfle. 2002. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30: e36.
61. Piel, J. 2002. A polyketide synthase-peptide synthetase gene cluster from an uncultured bacterial symbiont of Paederus beetles. Proc. Natl. Acad. Sci. USA 99: 14002-14007.
62. Piel, J., I. Hofer, and D. Hui. 2004. Evidence for a symbiosis island involved in horizontal acquisition of pederin biosynthetic capabilities by the bacterial symbiont of Paederus fuscipes beetles. J. Bacteriol. 186: 1280-1286.
63. Ridley, A. J., and A. Hall. 1992. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70: 389-399.
64. Rodriguez-Navarro, D. N., M. S. Dardanelli, and J. E. Ruiz-Sainz. 2007. Attachment of bacteria to the roots of higher plants. FEMS Microbiol. Lett. 272: 127-136.
65. Romling, U. 2002. Molecular biology of cellulose production in bacteria. Res. Microbiol. 153: 205-212.
66. Ross, P., R. Mayer, and M. Benziman. 1991. Cellulose biosynthesis and function in bacteria. Microbiol. Rev. 55: 35-58.
67. Rozen, S., and H. J. Skaletsky. 1998. Primer3. [Online] Code available at http://www-genome.wi.mit.edu/genome_software/other/primer3.html
68. Ruan, B. F., and H. L. Zhu. 2012. The chemistry and biology of the bryostatins: potential PKC inhibitors in clinical development. Curr. Med. Chem. 19: 2652-2664.
69. Ruby, E. G. 2008. Symbiotic conversations are revealed under genetic interrogation. Nat. Rev. Microbiol. 6: 752-762.
70. Ryland, J. S. 1970. Bryozoans. Hutchinson University Library, London
71. Sakon, J., D. Irwin, D. B. Wilson, and P. A. Karplus. 1997. Structure and mechanism of endo/exocellulase E4 from Thermomonospora fusca. Nat. Struct. Mol. Biol. 4: 810-818.
72. Scarborough, C. L., J. Ferrari, and H. Godfray. 2005. Aphid protected from pathogen by endosymbiont. Science 310: 1781.
73. Schmidt, E. W. 2008. Trading molecules and tracking targets in symbiotic interactions. Nat. Chem. Biol. 4: 466-473.
74. Sharp, K. H., S. K. Davidson, and M. G. Haygood. 2007. Localization of 'Candidatus Endobugula sertula' and the bryostatins throughout the life cycle of the bryozoan Bugula neritina. ISME J. 1: 693-702
75. Sieberer, B. J., A. C. J. Timmers, and A. M. C. Emons. 2005. Nod factors alter the microtubule cytoskeleton in Medicago truncatula root hairs to allow root hair reorientation. Mol. Plant Microbe Interact. 18: 1195-1204.
76. Stevens, L. M., M. R. Gregory, and B. A. Foster. 1996. Fouling Bryozoa on pelagic and moored plastics from northern New Zealand. Pp. 321-340 in Bryzoans in Space and Time, D. P. Gordon, A. M. Smith and J. A. Grant-Mackie, eds. National Institute of Water and Atmospheric Research, Wellington, New Zealand.
77. Stricker, S. A. 1989. Settlement and metamorphosis of the marine bryozoan Membranipora membranacea. Bull. Mar. Sci. 45: 387-405
78. Tamburri, M. N., and R. K. Zimmer-Faust. 1996. Suspension feeding: basic mechanisms controlling recognition and ingestion of larvae. Limnol. Oceanogr. 41: 1188-1197.
79. Ude, S., D. L. Arnold, C. D. Moon, T. Timms-Wilson, and A. J. Spiers. 2006. Biofilm formation and cellulose expression among diverse environmental Pseudomonas isolates. Environ. Microbiol. 8: 1997-2011.
80. Wendt, D. E. 2000. Energetics of larval swimming and metamorphosis in four species of Bugula (Bryozoa). Biol. Bull. 198: 346-356.
81. Wong, Y. H., S. M. Arellano, H. M. Zhang, T. Ravasi, and P. Y. Qian. 2010. Dependency on de novo protein synthesis and proteomic changes during metamorphosis of the marine bryozoan Bugula neritina. Proteome Sci. 8: 25.
82. Woollacott, R. 1981. Association of bacteria with bryozoan larvae. Mar. Biol. 65: 155-158.
83. Woollacott, R. M., and R. L. Zimmer. 1975. A simplified placenta-like system for the transport of extraembryonic nutrients during embryogenesis of Bugula neritina (bryozoa). J. Morphol. 147: 355-377
84. Zogaj, X., W. Bokranz, M. Nimtz, and U. Romling. 2003. Production of cellulose and curli fimbriae by members of the family Enterobacteriaceae isolated from the human gastrointestinal tract. Infect. Immun. 71: 4151-4158.