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The symbiotic complex of Dendroctonus simplex: implications in the beetle attack and its life cycle

Published online by Cambridge University Press:  26 February 2019

A.-A. Durand ,
P. Constant ,
E. Déziel  and
C. Guertin Open the ORCID record for C. Guertin [Opens in a new window]
A.-A. Durand
Affiliation:
INRS-Institut Armand Frappier, 531 Boul. Des Prairies, Laval, Québec, Canada, H7V 1B7
P. Constant
Affiliation:
INRS-Institut Armand Frappier, 531 Boul. Des Prairies, Laval, Québec, Canada, H7V 1B7
E. Déziel
Affiliation:
INRS-Institut Armand Frappier, 531 Boul. Des Prairies, Laval, Québec, Canada, H7V 1B7
C. Guertin*
Affiliation:
INRS-Institut Armand Frappier, 531 Boul. Des Prairies, Laval, Québec, Canada, H7V 1B7
*
*Author for correspondence Phone: (450) 687-5010 ext. 4117 Fax: (450) 686-5511 E-mail: [email protected]
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Abstract

The eastern larch beetle (Dendroctonus simplex Le Conte) is recognized as a serious destructive forest pest in the upper part of North America. Under epidemic conditions, this beetle can attack healthy trees, causing severe damages to larch stands. Dendroctonus species are considered as holobionts, as they engage in multipartite interactions with microorganisms, such as bacteria, filamentous fungi, and yeasts, which are implicated in physiological processes of the insect, such as nutrition. They also play a key role in the beetle's attack, as they are responsible for the detoxification of the subcortical environment and weaken the tree's defense mechanisms. The eastern larch beetle is associated with bacteria and fungi, but their implication in the success of the beetle remains unknown. Here, we investigated the bacterial and fungal microbiota of this beetle pest throughout its ontogeny (pioneer adults, larvae and pupae) by high-throughput sequencing. A successional microbial assemblage was identified throughout the beetle developmental stages, reflecting the beetle's requirements. These results indicate that a symbiotic association between the eastern larch beetle and some of these microorganisms takes place and that this D. simplex symbiotic complex is helping the insect to colonize its host tree and survive the conditions encountered.

Keywords

Dendroctonusdevelopmental stagesmicrobiotamicrobial communitieshigh throughput sequencing
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 109 , Issue 6 , December 2019 , pp. 723 - 732
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Copyright
Copyright © Cambridge University Press 2019 

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References

Adams, A.S. & Six, D.L. (2007) Temporal variation in mycophagy and prevalence of fungi associated with developmental stages of Dendroctonus ponderosae (Coleoptera: Curculionidae). Environmental Entomology 36, 64–72.Google Scholar
Adams, A.S., Six, D.L., Adams, S.M. & Holben, W.E. (2008) In vitro interactions between yeasts and bacteria and the fungal symbionts of the mountain pine beetle (Dendroctonus ponderosae). Microbial Ecology 56, 460–466.Google Scholar
Adams, A.S., Boone, C.K., Bohlmann, J. & Raffa, K.F. (2011) Responses of bark beetle-associated bacteria to host monoterpenes and their relationship to insect life histories. Journal of Chemical Ecology 37, 808–817.Google Scholar
Adams, A.S., Aylward, F.O., Adams, S.M., Erbilgin, N., Aukema, B.H., Currie, C.R., Suen, G. & Raffa, K.F. (2013) Mountain pine beetles colonizing historical and naïve host trees are associated with a bacterial community highly enriched in genes contributing to terpene metabolism. Applied and Environmental Microbiology 79, 3468–3475.Google Scholar
Bentz, B.J. & Six, D.L. (2006) Ergosterol content of fungi associated with Dendroctonus ponderosae and Dendroctonus rufipennis (Coleoptera: Curculionidae, Scolytinae). Annals of the Entomological Society of America 99, 189–194.Google Scholar
Boone, C.K., Keefover-Ring, K., Mapes, A.C., Adams, A.S., Bohlmann, J. & Raffa, K.F. (2013) Bacteria associated with a tree-killing insect reduce concentrations of plant defense compounds. Journal of Chemical Ecology 39, 1003–1006.Google Scholar
Bridges, J.R. (1981) Nitrogen-fixing bacteria associated with bark beetles. Microbial Ecology 7, 131–137.Google Scholar
Briones-Roblero, C.I., Rodriguez-Diaz, R., Santiago-Cruz, J.A., Zuniga, G. & Rivera-Orduna, F.N. (2017) Degradation capacities of bacteria and yeasts isolated from the gut of Dendroctonus rhizophagus (Curculionidae: Scolytinae). Folia Microbiologica (Praha) 62, 1–9.Google Scholar
Cale, J.A., Collignon, R.M., Klutsch, J.G., Kanekar, S.S., Hussain, A. & Erbilgin, N. (2016) Fungal volatiles can act as carbon sources and semiochemicals to mediate interspecific interactions among bark beetle-associated fungal symbionts. PLoS ONE 11, e0162197.Google Scholar
Cardoza, Y.J., Klepzig, K.D. & Raffa, K.F. (2006) Bacteria in oral secretions of an endophytic insect inhibit antagonistic fungi. Ecological Entomology 31, 636–645.Google Scholar
Chararas, C., Pignal, M.-C., Vodjdani, G. & Bourgeay-Causse, M. (1983) Glycosidases and B group vitamins produced by six yeasts strains from digestive tract of Phoracantha semipunctata larvae and their role in the insect development. Mycopathologia 83, 9–15.Google Scholar
Comeau, A.M., Harding, T., Galand, P.E., Vincent, W.F. & Lovejoy, C. (2012) Vertical distribution of microbial communities in a perennially stratified Arctic lake with saline, anoxic bottom waters. Scientific Reports 2, 1–10.Google Scholar
Davis, T.S. (2014) The ecology of yeasts in the bark beetle holobiont: a century of research revisited. Microbial Ecology 69, 723–732.Google Scholar
Davis, T.S. & Hofstetter, R.W. (2011) Reciprocal interactions between the bark beetle-associated yeast Ogataea pini and host plant phytochemistry. Mycologia 103, 1201–1207.Google Scholar
Davis, T.S., Hofstetter, R.W., Foster, J.T., Foote, N.E. & Keim, P. (2011) Interactions between the yeast Ogataea pini and filamentous fungi associated with the western pine beetle. Microbial Ecology 61, 626–634.Google Scholar
Durand, A.-A., Bergeron, A., Constant, P., Buffet, J.-P., Déziel, E. & Guertin, C. (2015) Surveying the endomicrobiome and ectomicrobiome of bark beetles: the case of Dendroctonus simplex. Scientific Reports 5, 17190.Google Scholar
Durand, A.-A., Buffet, J.-P., Constant, P., Déziel, E. & Guertin, C. (2017) Fungal communities associated with the eastern larch beetle: diversity and variation within developmental stages. BioRxiv 10.1101, 220780.Google Scholar
Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C. & Knight, R. (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics (Oxford, England) 27, 2194–2200.Google Scholar
Gibson, C.M. & Hunter, M.S. (2010) Extraordinarily widespread and fantastically complex: comparative biology of endosymbiotic bacterial and fungal mutualists of insects. Ecology Letters 13, 223–234.Google Scholar
Hernández-García, J.A., Briones-Roblero, C.I., Rivera-Orduña, F.N. & Zúñiga, GJSR. (2017) Revealing the gut bacteriome of Dendroctonus bark beetles (Curculionidae: Scolytinae): diversity, core members and co-evolutionary patterns. Scientific Reports 7, 13864.Google Scholar
Hofstetter, R.W., Dinkins-Bookwalter, J., Davis, T.S. & Klepzig, K.D. (2015) Symbiotic associations of bark beetles. in Vega, F.E. & Hofstetter, R.W. (Eds) Bark Beetles. Academic Press, San Diego, CA, USA.Google Scholar
Howe, M., Keefover-Ring, K. & Raffa, K.F. (2018) Pine engravers carry bacterial communities whose members reduce concentrations of host monoterpenes with variable degrees of redundancy, specificity, and capability. Environmental Entomology 47, 638–645.Google Scholar
Hu, X., Yu, J., Wang, C. & Chen, H. (2014) Cellulolytic bacteria associated with the gut of Dendroctonus armandi larvae (Coleoptera: Curculionidae: Scolytinae). Forests 5, 455–465.Google Scholar
Klepzig, K.D. & Six, D.L. (2004) Bark beetle-fungal symbiosis: context dependency in complex associations. Symbiosis 37, 189–205.Google Scholar
Kwong, W.K. & Moran, N.A. (2013) Cultivation and characterization of the gut symbionts of honey bees and bumble bees: description of Snodgrassella alvi gen. nov., sp. nov., a member of the family Neisseriaceae of the Betaproteobacteria, and Gilliamella apicola gen. nov., sp. nov., a member of Orbaceae fam. nov., Orbales ord. nov., a sister taxon to the order ‘Enterobacteriales’ of the Gammaproteobacteria. International Journal of Systematic and Evolutionary Microbiology 63, 2008–2018.Google Scholar
Langor, D.W. & Raske, A.G. (1987 a) Emergence, host attack, and overwintering behavior of the eastern larch beetle, Dendroctonus simplex LeConte (Coleoptera: Scolytidae), in Newfoundland. The Canadian Entomologist 119, 975–983.Google Scholar
Langor, D.W. & Raske, A.G. (1987 b) Reproduction and development of the eastern larch beetle, Dendroctonus simplex LeConte (Coleoptera: Scolytidae), in Newfoundland. The Canadian Entomologist 119, 985–992.Google Scholar
Langor, D.W. & Raske, A.G. (1989 a) The eastern larch beetle, another threat to our forests (Coleoptera: Scolytidae). Forestry Chronicle 65, 276–279.Google Scholar
Langor, D.W. & Raske, A.G. (1989 b) A history of the eastern larch beetle, Dendroctonus simplex (Coleoptera: Scolytidae), in North America. The Great Lakes Entomologist 22, 139–154.Google Scholar
Lieutier, F., Yart, A. & Salle, A. (2009) Stimulation of tree defenses by Ophiostomatoid fungi can explain attack success of bark beetles on conifers. Annals of Forest Science 66, 1–22.Google Scholar
Lu, M., Wingfield, M.J., Gillette, N. & Sun, J.H. (2011) Do novel genotypes drive the success of an invasive bark beetle-fungus complex? Implications for potential reinvasion. Ecology 92, 2013–2019.Google Scholar
Lu, M., Hulcr, J. & Sun, J. (2016) The role of symbiotic microbes in insect invasions. Annual Review of Ecology, Evolution, and Systematics 47, 487–505.Google Scholar
Margulis, L. & Fester, R. (1991) Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis. Mit Press, Cambridge, MA, USA.Google Scholar
Martin, K.J. & Rygiewicz, P.T. (2005) Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts. BMC Microbiology 5, 1–11.Google Scholar
Morales-Jimenez, J., Zuniga, G., Villa-Tanaca, L. & Hernandez-Rodriguez, C. (2009) Bacterial community and nitrogen fixation in the red turpentine beetle, Dendroctonus valens LeConte (Coleoptera: Curculionidae: Scolytinae). Microbial Ecology 58, 879–891.Google Scholar
Morales-Jimenez, J., Zuniga, G., Ramirez-Saas, H.C. & Heranadez-Rodriguez, C. (2012) Gut-associated bacteria throughout the life cycle of the bark beetle Dendroctonus rhizophagus Thomas and Bright (Curculionidae: Scolytinae) and their cellulolytic activities. Microbial Ecology 64, 268–278.Google Scholar
Morales-Jimenez, J., Vera-Ponce de León, A., García-Domínguez, A., Martínez-Romero, E., Zuniga, G. & Hernandez-Rodriguez, C. (2013) Nitrogen-fixing and uricolytic bacteria associated with the gut of Dendroctonus rhizophagus and Dendroctonus valens (Curculionidae: Scolytinae). Microbial Ecology 66, 200–210.Google Scholar
Mueller, U.G. & Gerardo, N.M. (2002) Fungus-farming insects: multiple origins and diverse evolutionary histories. PNAS 99, 15247–15249.Google Scholar
Mueller, U.G., Gerardo, N.M., Aanen, D.K., Six, D.L. & Schultz, T.R. (2005) The evolution of agriculture in insects. Annual Review of Ecology, Evolution, and Systematics 36, 563–595.Google Scholar
Paine, T.D., Raffa, K.F. & Harrington, T.C. (1997) Interactions among scolytid bark-beetles, their associated fungi, and live host conifers. Annual Review of Entomology 42, 179–206.Google Scholar
Popa, V., Déziel, E., Lavallée, R., Bauce, E. & Guertin, C. (2012) The complex symbiotic relationships of bark beetles with microorganisms: a potential practical approach for biological control in forestry. Pest Management Science 68, 963–975.Google Scholar
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J. & Glöckner, F.O. (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41, D590–D596.Google Scholar
Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J., Sahl, J.W., Stres, B., Thallinger, G.G., Van Horn, D.J. & Weber, C.F. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75, 7537–7541.Google Scholar
Schmitt, S., Tsai, P., Bell, J., Fromont, J., Ilan, M., Lindquist, N., Perez, T., Rodrido, A., Schupp, P.J., Vacelet, J., Webster, N.S., Hentschel, U. & Taylor, M.W. (2012) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. The ISME Journal 6, 564–576.Google Scholar
Scott, J.J., Oh, D.C., Yuceer, M.C., Klepzig, K.D., Clardy, J. & Currie, C.R. (2008) Bacterial protection of beetle-fungus mutualism. Science 322, 63.Google Scholar
Six, D.L. (2003) Bark beetle fungus symbioses. pp. 97–114, vol. 1 in Bourtzis, K. & Miller, T.A. (Eds) Insect Symbiosis. CRC Press LLC, Boca Raton, FL, USA.Google Scholar
Six, D.L. (2013) The bark beetle holobiont: why microbes matter. Journal of Chemical Ecology 39, 989–1002.Google Scholar
Six, D.L. & Wingfield, M.J. (2011) The role of phytopathogenicity in bark beetle–fungus symbioses: a challenge to the Classic Paradigm. Annual Review of Entomology 56, 255–272.Google Scholar
Wang, Q., Garrity, G.M., Tiedje, J. & Cole, J.R. (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73, 5261–5267.Google Scholar
Wang, S., Zhou, F., Wang, B., Xu, D., Cao, Q., Lu, M. & Sun, J.J.S.C.L.S. (2017) Volatiles produced by bacteria alleviate antagonistic effects of one associated fungus on Dendroctonus valens larvae. Science China Life Science 60, 924–926.Google Scholar
Winder, R.S., Macey, D.E. & Cortese, J. (2010) Dominant bacteria associated with broods of mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Curculionidae, Scolytinae). Journal of the Entomological Society of British Columbia 107, 43–56.Google Scholar
Wood, S.L. (2007) Bark and Ambroza Beetles of South America (Coleoptera: Scolytidae). Provo, Utah, USA, Brigham Young University, 900 p.Google Scholar
Xu, L., Deng, J., Zhou, F., Cheng, C., Zhang, L., Zhang, J. & Lu, M. (2019) Gut microbiota in an invasive bark beetle infected by a pathogenic fungus accelerates beetle mortality. Journal of Pesticide Science 92, 343–351.Google Scholar
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