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 AiM  Vol.6 No.8 , July 2016
Impact of the Glucosinolate Sinigrin on Bacterial Communities in Pieris rapae
Abstract: Dynamics in animal-associated microbiota can be difficult to study due to community complexity. Previous work showed that microbial communities in the midguts of Pieris rapae larvae contain relatively few members. In this study, we used P. rapae to test hypotheses related to how diet impacts gastrointestinal microbiota. More specifically, we investigated how the concentration of sinigrin, a glucosinolate in the natural diet of this insect, alters microbial community structure. Larvae were fed either sterile wheat germ diet alone or amended with 3.0 mg/ml, 6.0 mg/ml, or 9.0 mg/ml of sinigrin. In order to determine shifts in the gut microbial community, 16S rRNA genes from midguts were subjected to pyrosequencing and analyzed. Sinigrin had a significant impact on microbial communities in fourth instar P. rapae larvae, but this was dependent on concentration. The predominant phyla in all treatment groups were Proteobacteria and Firmicutes. Significant difference in beta diversity was typically observed when sinigrin 6 mg/ml and the control treatment groups were compared. The impact of sinigrin on the structure of the midgut microbiota is dependent on concentration, but not in a linear fashion. This may indicate that types and concentrations of glucosinolates have varied impact on midgut microbial community.
Cite this paper: McKinnon, L. and Robinson, C. (2016) Impact of the Glucosinolate Sinigrin on Bacterial Communities in Pieris rapae. Advances in Microbiology, 6, 566-573. doi: 10.4236/aim.2016.68057.
References

[1]   Little, A.E.F., Robinson, C.J., Peterson, S.B., Raffa, K.F. and Handelsman, J. (2008) Rules of Engagement: Interspecies Interactions That Regulate Microbial Communities. Annual Review of Microbiology, 62, 375-401.
http://dx.doi.org/10.1146/annurev.micro.030608.101423

[2]   Robinson, C.J., Bohannan, B.J.M. and Young, V.B. (2010) From Structure to Function: The Ecology of Host-Associated Microbial Communities. Microbiology and Molecular Biology Reviews, 74, 453-476.
http://dx.doi.org/10.1128/MMBR.00014-10

[3]   Handelsman, J., Robinson, C.J. and Raffa, K.F. (2005) Microbial Communities in Lepidopteran Guts: From Models to Metagenomics. In: McFall-Ngai, M.J., Henderson, B. and Ruby, E.G., Eds., Influence of Cooperative Bacteria on Animal Host Biology, Cambridge University Press, Cambridge, 143-168.

[4]   Dillon, R.J. and Dillon, V.M. (2004) The Gut Bacteria of Insects: Nonpathogenic Interactions. Annual Review of Entomology, 49, 71-92.
http://dx.doi.org/10.1146/annurev.ento.49.061802.123416

[5]   Engel, P. and Moran, N.A. (2013) The Gut Microbiota of Insects-Diversity in Structure and Function. FEMS Microbiology Reviews, 37, 699-735.
http://dx.doi.org/10.1111/1574-6976.12025

[6]   Kostic, A.D., Howitt, M.R. and Garrett, W.S. (2013) Exploring Host-Microbiota Interactions in Animal Models and Humans. Genes & Development, 27, 701-718.
http://dx.doi.org/10.1101/gad.212522.112

[7]   Dillon, R. and Charnley, K. (2002) Mutualism between the Desert Locust Schistocerca gregaria and Its Gut Microbiota. Research in Microbiology, 153, 503-509.
http://dx.doi.org/10.1016/s0923-2508(02)01361-x

[8]   Kane, M.D. and Breznak, J.A. (1991) Effect of Host Diet on Production of Organic Acids and Methane by Cockroach Gut Bacteria. Applied and Environmental Microbiology, 57, 2628-2634.

[9]   Brauman, A., Doré, J., Eggleton, P., Bignell, D., Breznak, J.A. and Kane, M.D. (2001) Molecular Phylogenetic Profiling of Prokaryotic Communities in Guts of Termites with Different Feeding Habits. FEMS Microbiology Ecology, 35, 27-36.
http://dx.doi.org/10.1111/j.1574-6941.2001.tb00785.x

[10]   Lundgren, J.G. and Lehman, R.M. (2010) Bacterial Gut Symbionts Contribute to Seed Digestion in an Omnivorous Beetle. PLOS ONE.

[11]   Douglas, A.E. (1998) Nutritional Interactions in Insect-Microbial Symbioses: Aphids and Their Symbiotic Bacteria Buchnera. Annual Review of Entomology, 43, 17-37.
http://dx.doi.org/10.1146/annurev.ento.43.1.17

[12]   Douglas, A.E. (2013) Microbial Brokers of Insect-Plant Interactions Revisited. Journal of Chemical Ecology, 39, 952-961.
http://dx.doi.org/10.1007/s10886-013-0308-x

[13]   Feldhaar, H. (2011) Bacterial Symbionts as Mediators of Ecologically. Ecological Entomology, 36, 533-543.
http://dx.doi.org/10.1111/j.1365-2311.2011.01318.x

[14]   Hammer, T.J. and Bowers, M.D. (2015) Gut Microbes May Facilitate Insect Herbivory of Chemically Defended Plants. Oecologia, 179, 1-14.
http://dx.doi.org/10.1007/s00442-015-3327-1

[15]   Mason, C.J. and Raffa, K.F. (2014) Acquisition and Structuring of Midgut Bacterial Communities in Gypsy Moth (Lepidoptera: Erebidae) Larvae. Environmental Entomology, 43, 595-604.
http://dx.doi.org/10.1603/EN14031

[16]   Broderick, N.A., Raffa, K.F., Goodman, R.M. and Handelsman, J. (2004) Census of the Bacterial Community of the Gypsy Moth Larval Midgut by Using Culturing and Culture-Independent Methods. Applied and Environmental Microbiology, 70, 293-300.
http://dx.doi.org/10.1128/AEM.70.1.293-300.2004

[17]   Robinson, C.J., Schloss. P.D., Ramos, Y., Raffa, K.F. and Handelsman, J. (2010) Robustness of the Bacterial Community in the Cabbage White Butterfly Larval Midgut. Microbial Ecology, 59, 199-211.
http://dx.doi.org/10.1007/s00248-009-9595-8

[18]   Liebhold, A.M., Gottschalk, K.W., Muzikam, R.-M., Montgomery, M.E., Young R., O’Day, K. and Kelley, B. (1995) Suitability of North American Tree Species to the Gypsy Moth: A Summary of Field and Laboratory Tests. USDA Forest Service, 1-36.

[19]   Fahey, J.W., Zalcmann, A.T. and Talalay, P. (2001) The Chemical Diversity and Distribution of Glucosinolates and Isothiocyanates among Plants. Phytochemistry, 56, 5-51.
http://dx.doi.org/10.1016/S0031-9422(00)00316-2

[20]   Mason, C.J., Rubert-Nason, K.F., Lindroth, R.L. and Raffa, K.F. (2014) Aspen Defense Chemicals Influence Midgut Bacterial Community Composition of Gypsy Moth. Journal of Chemical Ecology, 41, 75-84.
http://dx.doi.org/10.1007/s10886-014-0530-1

[21]   Müller, R., de Vos, M., Sun, J.Y., Sonderby, I.E., Halkier, B.A., Wittstock, U. and Jander, G. (2010) Differential Effects of Indole and Aliphatic Glucosinolates on Lepidopteran Herbivores. Journal of Chemical Ecology, 36, 905-913.
http://dx.doi.org/10.1007/s10886-010-9825-z

[22]   Wittstock, U., Agerbirk, N., Stauber, E.J., Olsen, C.E., Hippler, M., Mitchell-Olds, T., Gershenzon, J. and Vogel, H. (2004) Successful Herbivore Attack due to Metabolic Diversion of a Plant Chemical Defense. Proceedings of the National Academy of Sciences of the United States of America, 101, 4859-4864.
http://dx.doi.org/10.1073/pnas.0308007101

[23]   Kos, M., Houshyani, B., Wietsma, R., Kabouw, P., Vet, L.E.M., van Loon, J.J.A. and Dicke, M. (2012) Effects of Glucosinolates on a Generalist and Specialist Leaf-Chewing Herbivore and an Associated Parasitoid. Phytochemistry, 77, 162-170.
http://dx.doi.org/10.1016/j.phytochem.2012.01.005

[24]   Kozich, J.J., Westcott, S.L., Baxter, N.T., Highlander, S.K. and Schloss, P.D. (2013) Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform. Applied and Environmental Microbiology, 79, 5112-5120.
http://dx.doi.org/10.1128/AEM.01043-13

[25]   Koenigsknecht, M.J., Theriot, C.M., Bergin, I.L., Schumacher, C.A., Schloss, P.D. and Young, V.B. (2015) Dynamics and Establishment of Clostridium Difficile Infection in the Murine Gastrointestinal Tract. Infection and Immunity, 83, 934-941.
http://dx.doi.org/10.1128/IAI.02768-14

[26]   Schloss, P.D., Westcott, S.L., Ryabin, T., et al. (2009) Introducing Mothur: Open Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities. Applied and Environmental Microbiology, 75, 7537-7541.
http://dx.doi.org/10.1128/AEM.01541-09

[27]   Yue, J.C. and Clayton, M.K. (2005) A Similarity Measure Based on Species Proportions. Communications in Statistics—Theory and Methods, 34, 2123-2131.
http://dx.doi.org/10.1080/STA-200066418

[28]   White, J.R., Nagarajan, N. and Pop, M. (2009) Statistical Methods for Detecting Differentially Abundant Features in Clinical Metagenomic Samples. PLOS Computational Biology, 5, e1000352.
http://dx.doi.org/10.1371/journal.pcbi.1000352

[29]   Van Doorn, H.E., van Holst, G.-J., van der Kruk, G.C., Raaijmakers-Ruijs, N.C.M.E. and Postma, E. (1998) Quantitative Determination of the Glucosinolates Sinigrin and Progoitrin by Specific Antibody ELISA Assays in Brussels Sprouts. Journal of Agricultural and Food Chemistry, 46, 793-800.
http://dx.doi.org/10.1021/jf970523z

[30]   Walenciak, O., Zwisler, W. and Gross, E.M. (2002) Influence of Myriophyllum spicatum-Derived Tannins on Gut Microbiota of Its Herbivore Acentria ephemerella. Journal of Chemical Ecology, 28, 2045-2056.
http://dx.doi.org/10.1023/A:1020754012785

[31]   Shade, A., Peter, H., Allison, S.D., et al. (2012) Fundamentals of Microbial Community Resistance and Resilience. Frontiers in Microbiology, 3, 417.
http://dx.doi.org/10.3389/fmicb.2012.00417

[32]   Zhang, J., Friman, V.-P., Laakso, J. and Mappes, J. (2012) Interactive Effects between Diet and Genotypes of Host and Pathogen Define the Severity of Infection. Ecology and Evolution, 2, 2347-2356.
http://dx.doi.org/10.1002/ece3.356

[33]   Agelopoulos, N.G., Dicke, M. and Posthumus, M.A. (1995) Role of Volatile Inforchemicals Emitted by Feces of Larvae in Host-Searching Behavior of Parasitoid Cotesia rubecula (Hymenoptera: Braconidae): A Behavioral and Chemical Study. Journal of Chemical Ecology, 21, 1789-1811.
http://dx.doi.org/10.1007/BF02033677

[34]   Giamoustaris, A. and Mithen, R. (1995) The Effect of Modifying the Glucosinolate Content of Leaves of Oilseed Rape (Brassica napus ssp. oleifera) on Its Interaction with Specialist and Generalist Pests. Annals of Applied Biology, 126, 347-363.
http://dx.doi.org/10.1111/j.1744-7348.1995.tb05371.x

[35]   Ojala, K., Julkunen-Tiitto, R., Lindstrom, L. and Mappes, J. (2005) Diet Affects the Immune Defense and Life-History Traits of an Arctiid Moth Parasemia plantaginis. Evolutionary Ecology Research, 7, 1153-1170.

[36]   Gols, R., Wagenaar, R., Burkovinszky, T., van Dam, N., Dicke, M., Bullock, J.M. and Harvey, J.A. (2008) Genetic Variation in Defense Chemistry in Wild Cabbages Affects Herbivores and Their Endoparasitoids. Ecology, 89, 1616-1626.
http://dx.doi.org/10.1890/07-0873.1

 
 
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