Subterranean termite prophylactic secretions and external antifungal defenses

Journal of Insect Physiology

Volumn 57, Issue 9, 2011, Pages 1259-1266

  Hamilton, Casey ^a   Lay, Frank ^a   Bulmer, Mark S ^a  

^a TOWSON UNIVERSITY   (United States)

Author keywords

1,3 Glucanase; Allogrooming; Gram negative bacteria binding protein; Innate immunity; Prophylaxis; Social insects

Indexed keywords

ANTIFUNGAL AGENT; GLUCAN 1,3 BETA GLUCOSIDASE; INSECT PROTEIN; PEPTIDE; TERMICIN;

ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOLOGICAL CONTROL; CHEMICAL BINDING; DISEASE TRANSMISSION; ENTOMOPATHOGENIC ORGANISM; ENZYME ACTIVITY; FUNGUS; IMMUNE RESPONSE; IMMUNITY; INFECTIOUS DISEASE; MORTALITY; PROTEIN; SECRETION; SOCIAL INSECT; SOIL MICROORGANISM; SUBTERRANEAN ENVIRONMENT; TERMITE;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; DRUG ANTAGONISM; HOST PATHOGEN INTERACTION; ISOPTERA; METABOLISM; METARHIZIUM; MOLECULAR GENETICS; PHYSIOLOGY; SECRETION; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; ANTIFUNGAL AGENTS; GLUCAN 1,3-BETA-GLUCOSIDASE; HOST-PATHOGEN INTERACTIONS; INSECT PROTEINS; ISOPTERA; METARHIZIUM; MOLECULAR SEQUENCE DATA; PEPTIDES; SEQUENCE ALIGNMENT;

FUNGI; HEXAPODA; ISOPTERA; METARHIZIUM ANISOPLIAE; NEGIBACTERIA; RETICULITERMES FLAVIPES; RETICULITERMES VIRGINICUS; RHINOTERMITIDAE;

EID: 80052267719     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2011.05.016     Document Type: Article

References (41)

1. Bragatto I., Genta F.A., Ribeiro A.F., Terra W.R., Ferreira C. Characterization of a β-1,3-glucanase active in the alkaline midgut of Spodoptera frugiperda larvae and its relation to β-glucan-binding proteins. Insect Biochemistry and Molecular Biology 2010, 40:861-872.
2. Bulmer M.S., Crozier R.H. Variation in positive selection in termite GNBPs and relish. Molecular Biology and Evolution 2006, 23:317-326.
3. Bulmer M.S., Adams E.S., Traniello J.F.A. Variation in colony structure in the subterranean termite Reticulitermes flavipes. Behavioral Ecology and Sociobiology 2001, 49:236-243.
4. Bulmer M.S., Bachelet I., Raman R., Rosengaus R.B., Sasisekharan R. Targeting an antimicrobial effector function in insect immunity as a pest control strategy. Proceedings of the National Academy of Sciences, USA 2009, 106:12652-12657.
5. Bulmer M.S., Lay F., Hamilton C. Adaptive evolution in subterranean termite antifungal peptides. Insect Molecular Biology 2010, 19:669-674.
6. Chouvenc T., Su N.-Y., Elliott M.L. Interaction between the subterranean termite Reticulitermes flavipes (Isoptera: Rhinotermitidae) and the entomopathogenic fungus Metarhizium anisopliae in foraging arenas. Journal of Economic Entomology 2008, 101:885-893.
7. Chouvenc T., Su N.-Y., Robert A. Inhibition of Metarhizium anisopliae in the alimentary tract of the eastern subterranean termite Reticulitermes flavipes. Journal of Invertebrate Pathology 2009, 101:130-136.
8. Cremer S., Armitage S.A.O., Schmid-Hempel P. Social immunity. Current Biology 2007, 17:R693-R702.
9. Da Silva P., Jouvensal L., Lamberty M., Bulet P., Caille A., Vovelle F. Solution structure of termicin, an antimicrobial peptide from the termite Pseudacanthotermes spiniger. Protein Science 2003, 12:438-446.
10. Fefferman N.H., Traniello J.F.A., Rosengaus R.B., Calleri D.V. Disease prevention and resistance in social insects: modeling the survival consequences of immunity, hygienic behavior, and colony organization. Behavioral Ecology and Sociobiology 2007, 61:565-577.
11. Genta F.A., Bragatto I., Terra W.R., Ferreira C. Purification, characterization and sequencing of the major β-1,3-glucanase from the midgut of Tenebrio molitor larvae. Insect Biochemistry and Molecular Biology 2009, 39:861-874.
12. Gillespie J.P., Bailey A.M., Cobb B., Vilcinskas A. Fungi as elicitors of insect immune responses. Archives of Insect Biochemistry and Physiology 2000, 44:49-68.
13. Hughes W.O.H., Thomsen L., Eilenberg J., Boomsma J.J. Diversity of entomopathogenic fungi near leaf-cutting ant nests in a neotropical forest, with particular reference to Metarhizium anisopliae var Anisopliae. Journal of Invertebrate Pathology 2004, 85:46-53.
14. Juncosa M., Pons J., Dot T., Querol E., Planas A. Identification of active site carboxylic residues in Bacillus licheniformis 1,3-1,4-β-d-glucan 4-glucanohydrolase by site-directed mutagenesis. The Journal of Biological Chemistry 1994, 269:14530-14535.
15. Kalix S., Buchenauer H. Direct detection of β-1,3-glucanase in plant extracts by polyacrylamide gel electrophoresis. Electrophoresis 1995, 16:1016-1018.
16. Kim Y.-S., Ryu J.-H., Han S.-J., Choi K.-H., Nam K.-B., Jang I.-H., Lemaitre B., Brey P.T., Lee W.-J. Gram-negative bacteria-binding protein, a pattern recognition receptor for lipopolysaccharide and β-1,3-glucan that mediates the signaling for the induction of innate immune genes in Drosophila melanogaster cells. The Journal of Biological Chemistry 2000, 275:32721-32727.
17. Lamberty M., Zachary D., Lanot R., Bordereau C., Robert A., Hoffmann J.A., Bulet P. Insect immunity. Constitutive expression of a cysteine-rich antifungal and a linear antibacterial peptide in a termite insect. The Journal of Biological Chemistry 2001, 276:4085-4092.
18. Ma C., Kanost M.R. A β1,3-glucan recognition protein from an insect, Manduca sexta, agglutinates microorganisms and activates the phenoloxidase cascade. The Journal of Biological Chemistry 2000, 275:7505-7514.
19. Mellroth P., Steiner H. PGRP-SB1: an N-acetylmuramoyl l-alanine amidase with antibacterial activity. Biochemical and Biophysical Research Communications 2006, 350:994-999.
20. Ochiai M., Ashida M. A pattern-recognition protein for β-1,3-glucan. The binding domain and the cDNA cloning of β-1,3-glucan recognition protein from the silkworm, Bombyx mori. The Journal of Biological Chemistry 2000, 275:4995-5002.
21. Pauchet Y., Freitak D., Heidel-Fischer H.M., Heckel D.G., Vogel H. Immunity or digestion: glucanase activity in a glucan-binding protein family from Lepidoptera. Journal of Biological Chemistry 2009, 284:2214-2224.
22. Polizzi J.M., Forschler B.T. Intra- and interspecific agonism in Reticulitermes flavipes (Kollar) and R. Virginicus (Banks) and effects of arena and group size in laboratory assays. Insectes Sociaux 1998, 45:43-49.
23. Poulsen M., Bot A.N.M., Nielsen M.G., Boomsma J.J. Experimental evidence for the costs and hygienic significance of the antibiotic metapleural gland secretion in leaf-cutting ants. Behavioral Ecology and Sociobiology 2002, 52:151-157.
24. Rollins-Smith L.A., Reinert L.K., O'Leary C.J., Houston L.E., Woodhams D.C. Antimicrobial peptide defenses in amphibian skin. Integrative and Comparative Biology 2005, 45:137-142.
25. Rosengaus R.B., Maxmen A.B., Coates L.E., Traniello J.F.A. Disease resistance. a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera: Termopsidae). Behavioral Ecology and Sociobiology 1998, 44:125-134.
26. Rosengaus R.B., Traniello J.F.A., Lefebvre M.L., Maxmen A.B. Fungistatic activity of the sternal gland secretion of the dampwood termite Zootermopsis angusticollis. Insectes Sociaux 2004, 51:259-264.
27. Rosengaus R.B., Traniello J.F.A., Bulmer M.S. Ecology, behavior and evolution of disease resistance in termites. Biology of Termites: A Modern Synthesis 2011, 165-191. Springer, New York. D.E. Bignell, Y. Roisin, N. Lo (Eds.).
28. Royet J. Infectious non-self recognition in invertebrates: lessons from Drosophila and other insect models. Molecular Immunology 2004, 41:1063-1075.
29. Schlüns H., Crozier R.H. Molecular and chemical immune defenses in ants (Hymenoptera: Formicidae). Myrmecological News 2009, 12:237-249.
30. Sponsler R.C., Appeal A.G. Aspects of water relations of the Formosan and eastern subterranean termites (Isoptera: Rhinotermitidae). Environmental Entomology 1990, 19:15-20.
31. Strand M.R. The insect cellular immune response. Insect Science 2008, 15:1-14.
32. Todaka N., Moriya S., Saita K., Hondo T., Kiuchi I., Takasu H., Ohkuma M., Piero C., Hayashizaki Y., Kudo T. Environmental cDNA analysis of the genes involved in lignocellulose digestion in the symbiotic protist community of Reticulitermes speratus. FEMS Microbiology Ecology 2007, 59:592-599.
33. Vargo E.L. Hierarchical analysis of colony and population genetic structure of the eastern subterranean termite, Reticulitermes flavipes, using two classes of molecular markers. Evolution 2003, 57:2805-2818.
34. Vargo E.L., Husseneder C. Genetic structure of termite colonies. Biology of Termites: A Modern Synthesis 2011, 321-346. Springer, New York. D.E. Bignell, Y. Roisin, N. Lo (Eds.).
35. Vey A., Matha V., Dumas C. Effects of the peptide mycotoxin destruxin E on insect haemocytes and on dynamics and efficiency of the multicellular immune reaction. Journal of Invertebrate Pathology 2002, 80:177-187.
36. Wang C., St Leger R.J. A collagenous protective coat enables Metarhizium anisopliae to evade insect immune responses. Proceedings of the National Academy of Sciences, USA 2006, 103:6647-6652.
37. Warnecke F., Luginbühl P., Ivanova N., Chassemian M., Richardson T.H., Stege J.T., Cayouette M., McHardy A.C., Djordjevic G., Aboushadi N., Sorek R., Tringe S.G., Podar M., Martin H.G., Kunin V., Dalevi D., Madejska J., Kirton E., Platt D., Szeto E., Salamov A., Barry K., Mikhailova N., Kyrpides N.C., Matson E.G., Ottesen E.A., Zhang X., Hernández M., Murillo C., Acosta L.G., Rigoutsos I., Tamayo G., Green B.D., Chang C., Rubin E.M., Mathur E.J., Roberston D.E., Hugenholtz P., Leadbetter J.R. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 2007, 450:560-565.
38. Warr E., Das S., Dong Y., Dimopoulos G. The Gram-negative bacteria-binding protein gene family: its role in the innate immune system of Anopheles gambiae and in anti-Plasmodium defence. Insect Molecular Biology 2008, 17:39-51.
39. Yuki M., Moriya S., Inoue T., Kudo T. Transcriptome analysis of the digestive organs of Hodotermopsis sjostedti, a lower termite that hosts mutualistic microorganisms in its hindgut. Zoological Science 2008, 25:401-406.
40. Zhang R., Cho H.Y., Kim H.S., Ma Y.G., Osaki T., Kawabata S., Söderhäll K., Lee B.L. Characterization and properties of a 1,3-β-d-glucan pattern recognition protein of Tenebrio molitor larvae that is specifically degraded by serine protease during prophenoloxidase activation. The Journal of Biological Chemistry 2003, 278:42072-42079.
41. Zoberi M.H. Metarhizium anisopliae, a fungal pathogen of Reticulitermes flavipes (Isoptera: Rhinotermitidae). Mycologia 1995, 87:354-359.