The influence of Acetobacter pomorum bacteria on the developmental progression of Drosophila suzukii via gluconic acid secretion.

Acetobacter pomorum Drosophila suzukii deleterious gluconic acid microbe

Journal

Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478

Informations de publication

Date de publication:
10 Nov 2023
Historique:
revised: 24 10 2023
received: 19 10 2022
accepted: 26 10 2023
medline: 10 11 2023
pubmed: 10 11 2023
entrez: 10 11 2023
Statut: aheadofprint

Résumé

Insects are rich in various microorganisms, which play diverse roles in affecting host biology. Although most Drosophila species prefer rotten fruits, the agricultural pest Drosophila suzukii attacks ripening fruits before they are harvested. We have reported that the microbiota has positive and negative impacts on the agricultural pest D. suzukii on nutrient-poor and -rich diets, respectively. On nutrient-poor diets, microbes provide protein to facilitate larval development. But how they impede D. suzukii development on nutrient-rich diets is unknown. Here we report that Acetobacter pomorum (Apo), a commensal bacterium in many Drosophila species and rotting fruit, has several detrimental effects in D. suzukii. Feeding D. suzukii larvae nutrient-rich diets containing live Apo significantly delayed larval development and reduced the body weight of emerged adults. Apo induced larval immune responses and downregulated genes of digestion and juvenile hormone metabolism. Knockdown of these genes in germ-free larvae reproduced Apo-like weakened phenotypes. Apo was confirmed to secrete substantial amounts of gluconic acid. Adding gluconic acid to the D. suzukii larval diet hindered larval growth and decreased adult body weight. Moreover, the dose of gluconic acid that adversely affected D. suzukii did not negatively affect Drosophila melanogaster, suggesting that D. suzukii is less tolerant to acid than D. melanogaster. Taken together, these findings indicate that D. suzukii is negatively affected by gluconic acid, which may explain why it prefers ripening fruit over Apo-rich rotting fruit. These results show an insect's tolerance to microbes can influence its ecological niche.

Identifiants

pubmed: 37947376
doi: 10.1111/mec.17202
doi:

Banques de données

RefSeq
['SRR19355775', 'SRR19355783']

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Fundamental Research Funds for the Central Universities
ID : KJQN202110
Organisme : National Key R&D Program of China
ID : 2022YFC2601000
Organisme : National Natural Science Foundation of China
ID : 32001905
Organisme : National Natural Science Foundation of China
ID : 32020103011
Organisme : Natural Science Foundation of Jiangsu Province
ID : BK20211213

Informations de copyright

© 2023 John Wiley & Sons Ltd.

Références

Asplen, M. K., Anfora, G., Biondi, G., Choi, D. S., Chu, D., Daane, K. M., Gibert, P., Gutierrez, A. P., Hoelmer, K. A., Hutchison, W. D., Isaacs, R., Jiang, Z. L., Kárpáti, Z. L., Kimura, M. T., Pascual, M., Philips, C. R., Plantamp, C., Ponti, L., Vétek, L., … Desneux, N. (2015). Invasion biology of spotted wing Drosophila (Drosophila suzukii): A global perspective and future priorities. Journal of Pest Science, 88, 469-494.
Atallah, J., Teixeira, L., Salazar, R., Zaragoza, G., & Kopp, A. (2014). The making of a pest: The evolution of a fruit-penetrating ovipositor in Drosophila suzukii and related species. Proceedings of the Royal Society B: Biological Sciences, 281, 20132840.
Attwood, M. M., van Dijken, J. P., & Pronk, J. T. (1991). Glucose metabolism and gluconic acid production by Acetobacter diazotrophicus. Journal of Fermentation and Bioengineering, 72, 101-105.
Bai, S., Yao, Z., Raza, M. F., Cai, Z., & Zhang, H. (2021). Regulatory mechanisms of microbial homeostasis in insect gut. Insect Science, 28, 286-301.
Baumann, P. (2005). Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annual Review of Microbiology, 59, 155-189.
Belloni, V., Galeazzi, A., Bernini, G., Mandrioli, M., Versace, E., & Haase, A. (2018). Evolutionary compromises to metabolic toxins: Ammonia and urea tolerance in Drosophila suzukii and Drosophila melanogaster. Physiology & Behavior, 191, 146-154.
Bennett, G. M., & Moran, N. A. (2015). Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole. Proceedings of the National Academy of Sciences of the United States of America, 112, 10169-10176.
Benoit, J. B., Vigneron, A., Broderick, N. A., Wu, Y., Sun, J. S., Carlson, J. R., Aksoy, S., & Weiss, B. L. (2017). Symbiont-induced odorant binding proteins mediate insect host hematopoiesis. eLife, 6, e19535.
Bing, X., Gerlach, J., Loeb, G., & Buchon, N. (2018). Nutrient-dependent impact of microbes on Drosophila suzukii development. mBio, 9, e02199-02117.
Bing, X.-L., Lu, Y.-J., Xia, C.-B., Xia, X., & Hong, X.-Y. (2020). Transcriptome of Tetranychus urticae embryos reveals insights into Wolbachia-induced cytoplasmic incompatibility. Insect Molecular Biology, 29, 193-204.
Bing, X.-L., Winkler, J., Gerlach, J., Loeb, G., & Buchon, N. (2021). Identification of natural pathogens from wild Drosophila suzukii. Pest Management Science, 77, 1594-1606.
Bing, X.-L., Zhao, D.-S., Sun, J.-T., Zhang, K.-J., & Hong, X.-Y. (2020). Genomic analysis of Wolbachia from Laodelphax striatellus (Delphacidae, Hemiptera) reveals insights into its “Jekyll and Hyde” mode of infection pattern. Genome Biology and Evolution, 12, 3818-3831.
Broderick, N. A., & Lemaitre, B. (2012). Gut-associated microbes of Drosophila melanogaster. Gut Microbes, 3, 307-321.
Brune, A. (2014). Symbiotic digestion of lignocellulose in termite guts. Nature Reviews Microbiology, 12, 168-180.
Buchon, N., Broderick, N. A., Poidevin, M., Pradervand, S., & Lemaitre, B. (2009). Drosophila intestinal response to bacterial infection: Activation of host defense and stem cell proliferation. Cell Host & Microbe, 5, 200-211.
Buchon, N., Osman, D., David, F. P., Fang, H. Y., Boquete, J. P., Deplancke, B., & Lemaitre, B. (2013). Morphological and molecular characterization of adult midgut compartmentalization in Drosophila. Cell Reports, 3, 1725-1738.
Buchon, N., Silverman, N., & Cherry, S. (2014). Immunity in Drosophila melanogaster from microbial recognition to whole-organism physiology. Nature Reviews Immunology, 14, 796-810.
Chandler, J. A., James, P. M., Jospin, G., & Lang, J. M. (2014). The bacterial communities of Drosophila suzukii collected from undamaged cherries. PeerJ, 2, e474.
Chandler, J. A., Morgan Lang, J., Bhatnagar, S., Eisen, J. A., & Kopp, A. (2011). Bacterial communities of diverse Drosophila species: Ecological context of a host-microbe model system. PLoS Genetics, 7, e1002272.
Chen, S., Zhou, Y., Chen, Y., & Gu, J. (2018). Fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 34, i884-i890.
Consuegra, J., Grenier, T., Baa-Puyoulet, P., Rahioui, I., Akherraz, H., Gervais, H., Parisot, N., da Silva, P., Charles, H., Calevro, F., & Leulier, F. (2020). Drosophila-associated bacteria differentially shape the nutritional requirements of their host during juvenile growth. PLoS Biology, 18, e3000681.
De Cal, A., Sandín-España, P., Martinez, F., Egüen, B., Chien-Ming, C., Lee, M. H., Melgarejo, P., & Prusky, D. (2013). Role of gluconic acid and pH modulation in virulence of Monilinia fructicola on peach fruit. Postharvest Biology and Technology, 86, 418-423.
De Mendiburu, F., & Simon, R. (2015). Agricolae - Ten years of an open source statistical tool for experiments in breeding, agriculture and biology. PeerJ PrePrints, 3, e1404v1401.
Deppenmeier, U., Hoffmeister, M., & Prust, C. (2002). Biochemistry and biotechnological applications of Gluconobacter strains. Applied Microbiology and Biotechnology, 60, 233-242.
Douglas, A. E. (1998). Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera. Annual Review of Entomology, 43, 17-37.
Dweck, H. K., Talross, G. J., Wang, W., & Carlson, J. R. (2021). Evolutionary shifts in taste coding in the fruit pest Drosophila suzukii. eLife, 10, e64317.
Erkosar, B., Defaye, A., Bozonnet, N., Puthier, D., Royet, J., & Leulier, F. (2014). Drosophila microbiota modulates host metabolic gene expression via IMD/NF-κB signaling. PLoS ONE, 9, e94729.
Feyereisen, R. (1999). Insect P450 enzymes. Annual Review of Entomology, 44, 507-533.
Gomes, R. J., Borges, M. F., Rosa, M. F., Castro-Gómez, R. J. H., & Spinosa, W. A. (2018). Acetic acid bacteria in the food industry: Systematics, characteristics and applications. Food Technology and Biotechnology, 56, 139-151.
Goodhue, R. E., Bolda, M., Farnsworth, D., Williams, J. C., & Zalom, F. G. (2011). Spotted wing Drosophila infestation of California strawberries and raspberries: Economic analysis of potential revenue losses and control costs. Pest Management Science, 67, 1396-1402.
Gowda, K., & Kuehn, S. (2022). Microbial biofilms: An ecological tale of Jekyll and Hyde. Current Biology, 32, R1349-R1351.
Green, J. E., Cavey, M., Médina Caturegli, E., Aigouy, B., Gompel, N., & Prud'homme, B. (2019). Evolution of ovipositor length in Drosophila suzukii is driven by enhanced cell size expansion and anisotropic tissue reorganization. Current Biology, 29, 2075-2082.e2076.
Hamby, K. A., Hernández, A., Boundy-Mills, K., & Zalom, F. G. (2012). Associations of yeasts with spotted-wing Drosophila (Drosophila suzukii; Diptera: Drosophilidae) in cherries and raspberries. Applied and Environmental Microbiology, 78, 4869-4873.
Hansen, A. K., & Moran, N. A. (2014). The impact of microbial symbionts on host plant utilization by herbivorous insects. Molecular Ecology, 23, 1473-1496.
Henriques, S. F., Dhakan, D. B., Serra, L., Francisco, A. P., Carvalho-Santos, Z., Baltazar, C., Elias, A. P., Anjos, M., Zhang, T., Maddocks, O. D. K., & Ribeiro, C. (2020). Metabolic cross-feeding in imbalanced diets allows gut microbes to improve reproduction and alter host behaviour. Nature Communications, 11, 4236.
Houtz, P., Bonfini, A., Bing, X., & Buchon, N. (2019). Recruitment of adult precursor cells underlies limited repair of the infected larval midgut in Drosophila. Cell Host & Microbe, 26, 412-425.e415.
Ju, J. F., Bing, X. L., Zhao, D. S., Guo, Y., Xi, Z., Hoffmann, A. A., Zhang, K. J., Huang, H. J., Gong, J. T., Zhang, X., & Hong, X. Y. (2020). Wolbachia supplement biotin and riboflavin to enhance reproduction in planthoppers. The ISME Journal, 14, 676-687.
Karageorgi, M., Bräcker, L. B., Lebreton, S., Minervino, C., Cavey, M., Siju, K. P., Grunwald Kadow, I. C., Gompel, N., & Prud'homme, B. (2017). Evolution of multiple sensory systems drives novel egg-laying behavior in the fruit pest Drosophila suzukii. Current Biology, 27, 847-853.
Knapp, L., Mazzi, D., & Finger, R. (2021). The economic impact of Drosophila suzukii: Perceived costs and revenue losses of Swiss cherry, plum and grape growers. Pest Management Science, 77, 978-1000.
Kornecki, J. F., Carballares, D., Tardioli, P. W., Rodrigues, R. C., Berenguer-Murcia, Á., Alcantara, A. R., & Fernandez-Lafuente, R. (2020). Enzyme production of d-gluconic acid and glucose oxidase: Successful tales of cascade reactions. Catalysis Science & Technology, 10, 5740-5771.
Kosakamoto, H., Yamauchi, T., Akuzawa-Tokita, Y., Nishimura, K., Soga, T., Murakami, T., Mori, H., Yamamoto, K., Miyazaki, R., Koto, A., Miura, M., & Obata, F. (2020). Local necrotic cells trigger systemic immune activation via gut microbiome dysbiosis in Drosophila. Cell Reports, 32, 107938.
Leitão-Gonçalves, R., Carvalho-Santos, Z., Francisco, A. P., Fioreze, G. T., Anjos, M., Baltazar, C., Elias, A. P., Itskov, P. M., Piper, M. D. W., & Ribeiro, C. (2017). Commensal bacteria and essential amino acids control food choice behavior and reproduction. PLoS Biology, 15, e2000862.
Liu, X., Hodgson, J. J., & Buchon, N. (2017). Drosophila as a model for homeostatic, antibacterial, and antiviral mechanisms in the gut. PLoS Pathogens, 13, e1006277.
Love, M. I., Huber, W., & Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550.
Martinez-Sañudo, I., Simonato, M., Squartini, A., Mori, N., Marri, L., & Mazzon, L. (2018). Metagenomic analysis reveals changes of the Drosophila suzukii microbiota in the newly colonized regions. Insect Science, 25, 833-846.
Massie, H. R., & Williams, T. R. (1979). Increased longevity of Drosophila melanogaster with lactic and gluconic acids. Experimental Gerontology, 14, 109-115.
Minakuchi, C., & Riddiford, L. M. (2006). Insect juvenile hormone action as a potential target of pest management. Journal of Pesticide Science, 31, 77-84.
Mokeev, V., Flaven-Pouchon, J., Wang, Y., Gehring, N., & Moussian, B. (2021). Ratio between lactobacillus plantarum and Acetobacter pomorum on the surface of Drosophila melanogaster adult flies depends on cuticle melanisation. BMC Research Notes, 14, 351.
Mori, B. A., Whitener, A. B., Leinweber, Y., Revadi, S., Beers, E. H., Witzgall, P., & Becher, P. G. (2017). Enhanced yeast feeding following mating facilitates control of the invasive fruit pest Drosophila suzukii. Journal of Applied Ecology, 54, 170-177.
Mounir, M., Shafiei, R., Zarmehrkhorshid, R., Hamouda, A., Ismaili Alaoui, M., & Thonart, P. (2016). Simultaneous production of acetic and gluconic acids by a thermotolerant Acetobacter strain during acetous fermentation in a bioreactor. Journal of Bioscience and Bioengineering, 121, 166-171.
Overend, G., Luo, Y., Henderson, L., Douglas, A. E., Davies, S. A., & Dow, J. A. (2016). Molecular mechanism and functional significance of acid generation in the Drosophila midgut. Scientific Reports, 6, 27242.
Paris, M., Boyer, R., Jaenichen, R., Wolf, J., Karageorgi, M., Green, J., Cagnon, M., Parinello, H., Estoup, A., Gautier, M., Gompel, N., & Prud'homme, B. (2020). Near-chromosome level genome assembly of the fruit pest Drosophila suzukii using long-read sequencing. Scientific Reports, 10, 11227.
Patro, R., Duggal, G., Love, M. I., Irizarry, R. A., & Kingsford, C. (2017). Salmon provides fast and bias-aware quantification of transcript expression. Nature Methods, 14, 417.
R Team C. (2022). R: A language and environment for statistical computing. R Foundation for Statistical Computing. http://www.R-project.org/
Ridley, E. V., Wong, A. C. N., Westmiller, S., & Douglas, A. E. (2012). Impact of the resident microbiota on the nutritional phenotype of Drosophila melanogaster. PLoS ONE, 7, e36765.
Ruxton, G. D., Wilkinson, D. M., Schaefer, H. M., & Sherratt, T. N. (2014). Why fruit rots: Theoretical support for Janzen's theory of microbe-macrobe competition. Proceedings of the Royal Society B: Biological Sciences, 281, 20133320.
Sannino, D. R., Dobson, A. J., Edwards, K., Angert, E. R., & Buchon, N. (2018). The Drosophila melanogaster gut microbiota provisions thiamine to its host. mBio, 9, e00155-00118.
Sansone, C. L., Cohen, J., Yasunaga, A., Xu, J., Osborn, G., Subramanian, H., Gold, B., Buchon, N., & Cherry, S. (2016). Microbiota-dependent priming of antiviral intestinal immunity in Drosophila. Cell Host & Microbe, 18, 571-581.
Sato, A., Tanaka, K. M., Yew, J. Y., & Takahashi, A. (2021). Drosophila suzukii avoidance of microbes in oviposition choice. Royal Society Open Science, 8, 201601.
Sherald, A. F., & Wright, T. R. F. (1974). The analog inhibitor, α-methyl dopa, as a screening agent for mutants elevating levels of dopa decarboxylase activity in Drosophila melanogaster. Molecular and General Genetics MGG, 133, 25-36.
Shin, S. C., Kim, S. H., You, H., Kim, B., Kim, A. C., Lee, K. A., Yoon, J. H., Ryu, J. H., & Lee, W. J. (2011). Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science, 334, 670-674.
Solomon, G. M., Dodangoda, H., McCarthy-Walker, T., Ntim-Gyakari, R., & Newell, P. D. (2019). The microbiota of Drosophila suzukii influences the larval development of Drosophila melanogaster. PeerJ, 7, e8097.
Storelli, G., Defaye, A., Erkosar, B., Hols, P., Royet, J., & Leulier, F. (2011). Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metabolism, 14, 403-414.
Vacchini, V., Gonella, E., Crotti, E., Prosdocimi, E. M., Mazzetto, F., Chouaia, B., Callegari, M., Mapelli, F., Mandrioli, M., Alma, A., & Daffonchio, D. (2017). Bacterial diversity shift determined by different diets in the gut of the spotted wing fly Drosophila suzukii is primarily reflected on acetic acid bacteria. Environmental Microbiology Reports, 9, 91-103.
Wagner, S. M., Martinez, A. J., Ruan, Y. M., Kim, K. L., Lenhart, P. A., Dehnel, A. C., Oliver, K. M., & White, J. A. (2015). Facultative endosymbionts mediate dietary breadth in a polyphagous herbivore. Functional Ecology, 29, 1402-1410.
Walsh, D. B., Bolda, M. P., Goodhue, R. E., Dreves, A. J., Lee, J., Bruck, D. J., Walton, V. M., O'Neal, S. D., & Zalom, F. G. (2011). Drosophila suzukii (Diptera: Drosophilidae): Invasive pest of ripening soft fruit expanding its geographic range and damage potential. Journal of Integrated Pest Management, 2, G1-G7.
Wang, M., An, Y., Gao, L., Dong, S., Zhou, X., Feng, Y., Wang, P., Dimopoulos, G., Tang, H., & Wang, J. (2021). Glucose-mediated proliferation of a gut commensal bacterium promotes Plasmodium infection by increasing mosquito midgut pH. Cell Reports, 35, 108992.
Weisburg, W. G., Barns, S. M., Pelletier, D. A., & Lane, D. J. (1991). 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology, 173, 697-703.
Weiss, B. L., Maltz, M. A., Vigneron, A., Wu, Y., Walter, K. S., O'Neill, M. B., Wang, J., & Aksoy, S. (2019). Colonization of the tsetse fly midgut with commensal Kosakonia cowanii Zambiae inhibits trypanosome infection establishment. PLoS Pathogens, 15, e1007470.
Wong, C. N. A., Ng, P., & Douglas, A. E. (2011). Low-diversity bacterial community in the gut of the fruitfly Drosophila melanogaster. Environmental Microbiology, 13, 1889-1900.
Yu, G., Wang, L.-G., Han, Y., & He, Q.-Y. (2012). clusterProfiler: An R package for comparing biological themes among gene clusters. OMICS: A Journal of Integrative Biology, 16, 284-287.
Zhang, X., Li, S., & Liu, S. (2022). Juvenile hormone studies in Drosophila melanogaster. Frontiers in Physiology, 12, 785320.

Auteurs

Xiao-Li Bing (XL)

Department of Entomology, Nanjing Agricultural University, Nanjing, Jiangsu, China.

Zi-Jian Liang (ZJ)

Department of Entomology, Nanjing Agricultural University, Nanjing, Jiangsu, China.

Jia Tian (J)

Department of Entomology, Nanjing Agricultural University, Nanjing, Jiangsu, China.

Xue Gong (X)

Department of Entomology, Nanjing Agricultural University, Nanjing, Jiangsu, China.

Shao-Qiu Huang (SQ)

Department of Entomology, Nanjing Agricultural University, Nanjing, Jiangsu, China.

Jie Chen (J)

Department of Entomology, Nanjing Agricultural University, Nanjing, Jiangsu, China.

Xiao-Yue Hong (XY)

Department of Entomology, Nanjing Agricultural University, Nanjing, Jiangsu, China.

Classifications MeSH