Symbiont polyphyly, co-evolution, and necessity in pentatomid stinkbugs from Costa Rica

Frontiers in Microbiology

Volumn 5, Issue JULY, 2014, Pages

  Bistolas, Kalia S I ^a   Sakamoto, Reid I ^a   Fernandes, José A M ^b   Goffredi, Shana K ^a  

^a OCCIDENTAL COLLEGE   (United States)

^b FEDERAL UNIVERSITY OF PARÁ   (Brazil)

Author keywords

Erwinia; Neotropical; Pentatomid; Phytophagous; Stinkbug; Symbiosis

Indexed keywords

CYTOCHROME C OXIDASE;

ADULT; ARTICLE; COSTA RICA; EPIFLUORESCENCE MICROSCOPY; FLUORESCENCE IN SITU HYBRIDIZATION; INSECT; MORPHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; NYMPH; PHYLOGENETIC TREE; PHYLOGENY; POLYMERASE CHAIN REACTION; POLYPHYLY; SEQUENCE ALIGNMENT; STINKBUG; SYMBIONT; TRANSMISSION ELECTRON MICROSCOPY; UNINDEXED SEQUENCE;

EID: 84905400604     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00349     Document Type: Article

References (69)

1. Abe, Y., Mishiro, K., and Takanashi, M. (1995). Symbiont of brown-winged green bug Plautia stali Scott. Jpn. J. Appl. Entomol. Zool. 39, 109-115. doi: 10.1303/jjaez.39.109
2. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., et al. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402. doi: 10.1093/nar/25.17.3389
3. Amann, R. I., Binder, B. J., Olson, R. J., Chisholm, S. W., Devereux, R., and Stahl, D. A. (1990). Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 56, 1919-1925.
4. Buchner, P. (1965). Endosymbiosis of Animals with Plant Microorganisms. ed H. Malke. New York, NY: Interscience publ.
5. Corrêa-Ferreira, B. S., and de Azevedo, J. (2002). Soybean seed damage by different species of stink bugs. Agric. Forest Entomol. 4, 145-150. doi: 10.1046/j.1461-9563.2002.00136.x
6. Coupe, M. D., and Cahill, J. F. (2003). Effects of insects on primary production in temperate herbaceous communities: a meta-analysis. Ecol. Entomol. 28, 511-521. doi: 10.1046/j.1365-2311.2003.00540.x
7. Daims, H., Bruhl, A., Amann, R., Schleifer, K.-H., and Wagner, M. (1999). The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Syst. Appl. Microbiol. 22, 434-444. doi: 10.1016/S0723-2020(99)80053-8
8. de Vienne, D. M., Giraud, T., and Martin, O. C. (2007). A congruence index for testing topological similarity between trees. Bioinformatics 23, 3119-3124. doi: 10.1093/bioinformatics/btm500
9. Douglas, A. E. (1998). Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu. Rev. Ent. 43, 17-37. doi: 10.1146/annurev.ento.43.1.17
10. Douglas, A. E. (2009). The microbial dimension in insect nutritional ecology. Funct. Ecol. 23, 38-47. doi: 10.1111/j.1365-2435.2008.01442.x
11. Douglas, A. E. (2013). Microbial brokers of insect-plant interactions revisited. J. Chem. Ecol. 39, 952-961. doi: 10.1007/s10886-013-0308-x
12. Ferrari, J., and Vavre, F. (2011). Bacterial symbionts in insects or the story of communities affecting communities. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366, 1389-1400. doi: 10.1098/rstb.2010.0226
13. Fitzpatrick, B. M., Fordyce, J. A., and Gavrilets, S. (2008). What, if anything, is sympatric speciation? J. Evol. Biol. 21, 1452-1459. doi: 10.1111/j.1420-9101.2008.01611.x
14. Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3, 294-299.
15. Frago, E., Dicke, M., and Godfray, H. C. J. (2012). Insect symbionts as hidden players in insect-plant interactions. Trends. Ecol. Evol. 27, 705-711. doi: 10.1016/j.tree.2012.08.013
16. Fukatsu, T., and Hosokawa, T. (2002). Capsule-transmitted gut symbiotic bacterium of the Japanese common plataspid stinkbug, Megacopta punctatissima. Appl. Environ. Microbiol. 68, 389-396. doi: 10.1128/AEM.68.1.389-396.2002
17. Futahashi, R., Tanaka, K., Tanahashi, M., Nikoh, N., Kikuchi, Y., Lee, B. L., et al. (2013). Gene expression in gut symbiotic organ of stinkbug affected by extracellular bacterial symbiont. PLoS ONE 8:e64557. doi: 10.1371/journal.pone.0064557
18. García-Robledo, C., Erickson, D. L., Staines, C. L., Erwin, T. L., and Kress, J. W. (2013). Tropical Plant-herbivore networks: reconstructing species interactions using DNA barcodes. PLoS ONE 8:1. doi: 10.1371/journal.pone.0052967
19. Gilbert, L. E., and Smiley, J. T. (1978). "Determinants of local diversity in phytophageous insects: host specialists in tropical environments," in Diversity of Insect Faunas, eds L. A. Mound and N. Waloff (London: Symposia of the Royal Entomological Society of London), 89-103.
20. Golden, M., Follett, P. A., and Wright, M. G. (2006). Assessing Nezara viridula (Hemiptera: Pentatomidae) feeding damage in macadamia nuts by using a biological stain. J. Econ. Entomol. 99, 822-827. doi: 10.1603/0022-0493-99.3.822
21. Goodchild, A. J. P. (1963). Studies on the functional anatomy of the intestines of Heteroptera. Proc. Zool. Soc. Lond. 141, 851-910. doi: 10.1111/j.1469-7998.1963.tb01631.x
22. Greig, N. (1993). Predispersal seed predation on five Piper species in tropical rainforest. Oecologia 93, 412-420. doi: 10.1007/BF00317886
23. Hirose, E., Panizzi, A. R., and Prado, S. S. (2012). "Symbionts and nutrition of insects," in Insect Bioecology and Nutrition for Integrated Pest Management, eds A. R. Panizzi and J. R. P. Parra (Boca Raton, FL: CRC Press), 145-162. doi: 10.1201/b11713-8
24. Hokyo, N., and Kiritani, K. (1963). Mortality process in relation to aggregation in the Southern Green Stink Bug. Res. Popul. Ecol. 5, 23-30. doi: 10.1007/BF02518818
25. Hori, K. (2000). "Possible causes of disease symptoms resulting from the feeding of phytophagous heteroptera," in Heteroptera of Economic Importance, eds C. W. Schaefer and A. R. Panizzi (Boca Raton, FL: CRC Press), 11-36. doi: 10.1201/9781420041859.ch2
26. Hosokawa, T., Kikuchi, Y., Nikoh, N., and Fukatsu, T. (2012). Polyphyly of gut symbionts in stinkbugs of the family Cydnidae. Appl. Environ. Microbiol. 78, 4758-4761. doi: 10.1128/AEM.00867-12
27. Hosokawa, T., Kikuchi, Y., Nikoh, N., Meng, X. Y., Hironaka, M., and Fukatsu, T. (2010). Phylogenetic position and peculiar genetic traits of a midgut bacterial symbiont of the stinkbug Parastrachia japonensis. Appl. Environ. Microbiol. 76, 4130-4135. doi: 10.1128/AEM.00616-10
28. Hosokawa, T., Kikuchi, Y., Nikoh, N., Shimada, M., and Fukatsu, T. (2006). Strict host-symbiont cospeciation and reductive genome evolution in insect gut bacteria. PLoS Biol. 4:10. doi: 10.1371/journal.pbio.0040337
29. Hosokawa, T., Kikuchi, Y., Shimada, M., and Fukatsu, T. (2007). Obligate symbiont involved in pest status of host insect. Proc. Biol. Sci. 274, 1979-1984. doi: 10.1098/rspb.2007.0620
30. Joy, J. B. (2013). Symbiosis catalyses niche expansion and diversification. Proc. Biol. Sci. 280:20122820. doi: 10.1098/rspb.2012.2820
31. Kaiwa, N., Hosokawa, T., Kikuchi, Y., Nikoh, N., Meng, X. Y., Kimura, N., et al. (2010). Primary gut symbiont and secondary Sodalis-allied symbiont in the scutellerid stinkbug Cantao ocellatus. Appl. Environ. Microbiol. 76, 3486-3494. doi: 10.1128/AEM.00421-10
32. Kikuchi, Y., Hosokawa, T., Nikoh, N., and Fukatsu, T. (2012). Gut symbiotic bacteria in the cabbage bugs Eurydema rugosa and Eurydema dominulus (Heteroptera: Pentatomidae). Appl. Entomol. Zool. 47, 1-8 doi: 10.1007/s13355-011-0081-7
33. Kikuchi, Y., Hosokawa, T., Nikoh, N., Meng, X. Y., Kamagata, Y., and Fukatsu, T. (2009). Host-symbiont co-speciation and reductive genome evolution in gut symbiotic bacteria of acanthosomatid stinkbugs. BMC Biol. 7:2. doi: 10.1186/1741-7007-7-2
34. Klepzig, K. D. (2009). Symbioses: a key driver of insect physiological processes, ecological interactions, evolutionary diversification, and impacts on humans. Environ. Entomol. 38, 67-77. doi: 10.1603/022.038.0109
35. Kuechler, S. M., Dettner, K., and Kehl, S. (2011). Characterization of an obligate intracellular bacterium in the midgut epithelium of the Bulrush Bug Chilacis typhae (Heteroptera, Lygaeidae, Artheneinae). Appl. Environ. Microbiol. 77, 2869-2876. doi: 10.1128/AEM.02983-10
36. Kuriwada, T., Hosokawa, T., Kumano, N., Shiromoto, K., Haraguchi, D., and Fukatsu, T. (2010). Biological role of Nardonella endosymbiont in its weevil host. PLoS ONE 5:e13101. doi: 10.1371/journal.pone.0013101
37. Lane, D. J. (1991). "16S/23S rRNA sequencing," in Nucleic Acid Techniques in Bacterial Systematics, eds E. Stackebrandt and M. Goodfellow (New York, NY: John Wiley & Sons), 115-147.
38. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar Buchner, et al. (2004). ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363-1371. doi: 10.1093/nar/gkh293
39. Macalady, J. L., Lyon, E. H., Koffman, B., Albertson, L. K., Meyer, K., Galdenzi, S., et al. (2006). Dominant microbial populations in limestone-corroding stream biofilms, Frasassi Cave System, Italy. Appl. Environ. Microbiol. 72, 5596-5609. doi: 10.1128/AEM.00715-06
40. Manz, W., Amann, R., Ludwig, W., Wagner, M., and Schleifer, K.-H. (1992). Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: problems and solutions. Syst. Appl. Microbiol. 15, 593-600. doi: 10.1016/S0723-2020(11)80121-9
41. McDade, L. A., Bawa, K. S., Hespenheide, H. A., and Hartshorn, G. S. (1994). "Introduction: ecology and natural history of a neotropical rainforest," in La Selva: Ecology and Natural History of a Neotropical Rain Forest, ed L.A. McDade (Chicago, IL: University of Chicago Press), 261-281.
42. Metcalfe, D. B., Asner, G.,P., Martin, R. E., Silva Espejo, J. E., Huasco, W. H., and Malhi, Y. (2014). Herbivory makes major contributions to ecosystem carbon and nutrient cycling in tropical forests. Ecol. Lett. 17, 324-332. doi: 10.1111/ele.12233
43. Moran, N. A., Plague, G. R., Sandström, J. P., and Wilcox, J. L. (2003). A genomic perspective on nutrient provisioning by bacterial symbionts of insects. Proc. Natl. Acad. Sci. U.S.A. 100, 14543-14548. doi: 10.1073/pnas.2135345100
44. Nakabachi, A., and Ishikawa, H. (1999). Provision of riboflavin to the host aphid, Acyrthosiphon pisum, by endosymbiotic bacteria, Buchnera. J. Ins. Physiol. 45, 1-6. doi: 10.1016/S0022-1910(98)00104-8
45. Nikoh, N., Hosokawa, T., Oshima, K., Hattori, M., and Fukatsu, T. (2011). Reductive evolution of bacterial genome in insect gut environment. Genome Biol. Evol. 3, 702-714. doi: 10.1093/gbe/evr064
46. Pais, R., Lohs, C., Wu, Y., Wang, J., and Aksoy, S. (2008). The obligate mutualist Wigglesworthia glossinidia influences reproduction, digestion, and immunity processes of its host, the tsetse fly. Appl. Environ. Microbiol. 74, 5965-5974. doi: 10.1128/AEM.00741-08
47. Panizzi, A. R. (1997). Wild hosts of pentatomids: ecological significance and role in their pest status on crops. Annu. Rev. Entomol. 42, 99-122. doi: 10.1146/annurev.ento.42.1.99
48. Pernthaler, A., and Pernthaler, J. (2005). Simultaneous fluorescence in situ hybridization of mRNA and rRNA for the detection of gene expression in environmental microbes. Meth. Enzymol. 397, 352-371. doi: 10.1016/S0076-6879(05)97021-3
49. Prado, S. S., and Almeida, R. P. P. (2009a). Phylogenetic placement of pentatomid stink bug gut symbionts. Curr. Microbiol. 58, 64-69. doi: 10.1007/s00284-008-9267-9
50. Prado, S. S., and Almeida, R. P. P. (2009b). Role of symbiotic gut bacteria in the development of Acrosternum hilare and Murgantia histrionica. Entomol. Exp. Appl. 132, 21-29. doi: 10.1111/j.1570-7458.2009.00863.x
51. Prado, S. S., Golden, M., Follet, P. A., Daugherty, M. P., and Almeida, R. P. P. (2009). Demography of gut symbiotic and aposymbiotic Nezara viridula (L) (Hemiptera: Pentatomidae). Environ. Entomol. 38, 103-109. doi: 10.1603/022.038.0112
52. Prado, S. S., Hung, K. Y., Daugherty, M. P., and Almeida, R. P. (2010). Indirect effects of temperature on stink bug fitness, via maintenance of gut-associated symbionts. Appl. Environ. Microbiol. 76, 1261-1266. doi: 10.1128/AEM.02034-09
53. Prado, S. S., Rubinoff, D., and Almeida, R. P. P. (2006). Vertical transmission of a pentatomid caeca-associated symbiont. Ann. Entomol. Soc. Am. 99, 577-585. doi: 10.1603/0013-8746(2006)99[577:VTOAPC]2.0.CO;2
54. Prado, S. S., and Zucchi, T. D. (2012). Host-symbiont interactions for potentially managing heteropteran pests. Psyche 2012:269473. doi: 10.1155/2012/269473
55. Preusse, E., Quast, C., Knittel, K., Fuchs, B. M., Ludwig, W. G., Peplies, J., et al. (2007). SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35, 7188-7196. doi: 10.1093/nar/gkm864
56. Russell, J. A., Moreau, C. S., Goldman-Huertas, B., Fujiwara, M., Lohman, D. J., and Pierce, N. E. (2009). Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc. Natl. Acad. Sci. U.S.A. 106, 21236-21241. doi: 10.1073/pnas.0907926106
57. Schuh, R. T., and Slater, J. A. (1995). True Bugs of the World (Hemiptera: Heteroptera): Classification and natural history. Ithaca, NY: Cornell University Press, 336.
58. Shen, S. K., and Dowd, P. F. (1991). Detoxification spectrum of the cigarette beetle symbiont Symbiotaphrina kochii in culture. Entomol. Exp. Appl. 60, 51-59. doi: 10.1111/j.1570-7458.1991.tb01522.x
59. Silva, D. P., and Oliveria, P. S. (2010). Field biology of Edessa rufomarginata (Hemiptera: Pentatomidae): phenology, behavior, and patterns of host plant use. Environ. Entomol. 39: 1903-1910. doi: 10.1603/EN10129
60. Starr, M. P., and Chaterrjee, A. K. (1972). The genus Erwinia: enterobacteria pathogenic to plants and animals. Annu. Rev. Microbiol. 26, 389-426. doi: 10.1146/annurev.mi.26.100172.002133
61. Steedman, H. F. (1957). A new ribboning embedding medium for histology. Nature. 179, 1345. doi: 10.1038/1791345a0
62. Su, Q., Zhou, X., and Zhang, Y. (2013). Symbiont-mediated functions in insect hosts. Comm. Integr. Biol. 6, e23804. doi: 10.4161/cib.23804
63. Swofford, D. L. (1998). PAUP*: Phylogenetic Analysis Using Parsimony (*and other Methods) Version 4.0 (Prerelease Test Version). Sinauer, Sunderland, Mass.
64. Tada, T., Kikuchi, Y., Hosokawa, T., Musolin, D. L., Fujisaki, K., and Fukatsu, T. (2011). Obligate association with gut bacterial symbiont in Japanese populations of the southern green stinkbug Nezara viridula (Heteroptera: Pentatomidae). Appl. Entomol. Zool. 46, 483-488. doi: 10.1007/s13355-011-0066-6
65. Taylor, C. M., Coffey, P. L., DeLay, B. D., and Dively, G. P. (2014). The importance of gut symbionts in the development of the brown marmorated stink bug, Halyomorpha halys (Stål). PLoS ONE 9:e90312. doi: 10.1371/journal.pone.0090312
66. Urban, J. M., and Cryan, J. R. (2012). Two ancient bacterial endosymbionts have coevolved with the planthoppers (Insecta: Hemiptera: Fulgoroidea). BMC. Evol. Biol. 12:87. doi: 10.1186/1471-2148-12-87
67. Whitehead, S. R., and Bowers, M. D. (2014). Chemical ecology of fruit defense: synergistic and antagonistic interactions among amides from Piper. Funct. Ecol. doi: 10.1111/1365-2435.12250. [Epub ahead of print].
68. Wu, D., Daugherty, S. C., Van Aken, S. E., Pai, G. H., Watkins, K. L., Khouri, H. L., et al. (2006). Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol. 4:e188. doi: 10.1371/journal.pbio.0040188
69. Zucchi, T. D., Prado, S. S., and Cônsoli, F. L. (2012). The gastric caeca of pentatomids as a house for actinomycetes. BMC Microbiol. 12:101. doi: 10.1186/1471-2180-12-101