Spiroplasma affects host aphid proteomics feeding on two nutritional resources

[en] Bacterial symbionts are broadly distributed among insects, influencing their bioecology to different degrees. Aphids carry a number of secondary symbionts that can influence aphid physiology and fitness attributes. Spiroplasma is seldom reported as an aphid symbiont, but a high level of infection has been observed in one population of the tropical aphid Aphis citricidus. We used sister isolines of Spiroplasma-infected (Ac-BS) and Spiroplasma-free (Ac-B) aphids reared on sweet orange (optimum host) and orange jasmine (suboptimum host) to demonstrate the effects of Spiroplasma infection in the aphid proteome profile. A higher number of proteins were differently abundant in aphids feeding on orange jasmine, indicating an impact of host plant quality. In both host plants, the majority of proteins affected by Spiroplasma infection were heat shock proteins, proteins linked to cell function and structure, and energy metabolism. Spiroplasma also induced changes in proteins involved in antimicrobial activity, carbohydrate processing and metabolism, amino acid synthesis and metabolism in aphids feeding on orange jasmine. We discuss on how the aphid host proteome is differentially affected by Spiroplasma infection when the host is exploiting host plants with different nutritional values. © 2018 The Author(s).

Disciplines :

Entomology & pest control

Author, co-author :

Guidolin, A. S.; Insect Interactions Laboratory, Department of Entomology and Acarology, ESALQ, University of São Paulo, Av. Pádua Dias 11, São Paulo, Piracicaba, Brazil

Cataldi, T. R.; Max Feffer Laboratory of Plant Genetics, Department of Genetics, ESALQ, University of São Paulo, Av. Pádua Dias 11, São Paulo, Piracicaba, Brazil

Labate, C. A.; Max Feffer Laboratory of Plant Genetics, Department of Genetics, ESALQ, University of São Paulo, Av. Pádua Dias 11, São Paulo, Piracicaba, Brazil

Francis, Frédéric ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Gestion durable des bio-agresseurs

Cônsoli, F. L.; Insect Interactions Laboratory, Department of Entomology and Acarology, ESALQ, University of São Paulo, Av. Pádua Dias 11, São Paulo, Piracicaba, Brazil

Language :

English

Title :

Spiroplasma affects host aphid proteomics feeding on two nutritional resources

Publication date :

2018

Journal title :

Scientific Reports

eISSN :

2045-2322

Publisher :

Nature Publishing Group

Volume :

Issue :

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 12 November 2019

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Bibliography

Moran, N. A. Symbiosis as an adaptive process and source of phenotypic complexity. P. Natl. Acad. Sci. USA 104, 8627-8633 (2007).
Cilia, M. et al. Genetics coupled to quantitative intact proteomics links heritable aphid and endosymbiont protein expression to circulative polerovirus transmission. J. Virol. 85, 2148-2166 (2011).
Hansen, A. K. &Moran, N. A. The impact of microbial symbionts on host plant utilization by herbivorous insects. Molec. Ecol. 23, 1473-1496 (2014).
Buchner, P. Endosymbiosis of animals with plant microorganisms. (ed. Wiley, J) 909p (Interscience Publishers, 1965).
Douglas, A. E. Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria B. aphidicola. Ann. Rev. Entomol. 43, 17-37 (1998).
Chen, D. Q. &Purcell, A. H. Occurrence and transmission of facultative endosymbionts in aphids. Curr. Microbiol. 34, 220-225 (1997).
Tsuchida, T., Nikoh, N., Kawai, R. &Koga, R. Secondary endosymbiotic microbiota of the pea aphid, Acyrthosiphon pisum, in natural populations. Aphids in a New Millennium, 93-96 (2004).
Moran, N. A., Degnan, P. H., Santos, S. R., Dunbar, H. E. &Ochman, H. The players in a mutualistic symbiosis: Insects, bacteria, viruses, and virulence genes. P. Natl. Acad. Sci. USA 102, 16919-16926 (2005).
Douglas, A. E. Multiorganismal insects: diversity and function of resident microorganisms. Ann. Rev. Entomol. 60, 17-34 (2014).
Zytynska, S. E. &Weisser, W. W. The natural occurrence of secondary bacterial symbionts in aphids. Ecol. Entomol. 41, 13-26 (2016).
Chandler, S. M., Wilkinson, T. L. &Douglas, A. E. Impact of plant nutrients on the relationship between a herbivorous insect and its symbiotic bacteria. Proc. R. Soc. London-B 275, 565-570 (2008).
Su, Q., Zhou, X. &Zhang, Y. Symbiont-mediated functions in insect hosts. Commun. Integr. Biol. 6, 23804-23804 (2013).
McLean, A. H. C., van Asch, M., Ferrari, J. &Godfray, H. C. Effects of bacterial secondary symbionts on host plant use in pea aphids. Proc. R. Soc. London-B 278, 760-766 (2011).
Ferrari, J., West, J. A., Via, S. &Godfray, H. C. J. Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex. Evolution 66, 375-390 (2012).
Francis, F. et al. Proteomics in Myzus persicae: Effect of aphid host plant switch. Insect Biochem. Molec. Biol. 36, 219-227 (2006).
Nguyen, T. T. A., Michaud, D. &Cloutier, C. Proteomic profiling of aphid Macrosiphum euphorbiae responses to host-plantmediated stress induced by defoliation and water deficit. J. Insect Physiol. 53, 601-611 (2007).
Francis, F. et al. Tritrophic interactions among Macrosiphum euphorbiae aphids, their host plants and endosymbionts: Investigation by a proteomic approach. J. Insect Physiol. 56, 575-585 (2010).
Elzinga, D. A., De Vos, M. &Jander, G. Suppression of plant defenses by a Myzus persicae (Green Peach Aphid) salivary effector protein. Mol. Plant Microbe 27, 747-756 (2014).
Vandermoten, S. et al. Comparative analyses of salivary proteins from three aphid species. Insect Molec. Biol. 23, 67-77 (2014).
Gasparich, G. E. Spiroplasmas and Phytoplasmas: Microbes associated with plant hosts. Biologicals 38, 193-203 (2010).
Haselkorn, T. S. The Spiroplasma heritable bacterial endosymbiont of Drosophila. Fly 4, 80-87 (2010).
Ventura, I. M. et al. Spiroplasma in Drosophila melanogaster populations: prevalence, male-killing, molecular identification, and no association with Wolbachia. Microb. Ecol. 64, 794-801 (2012).
Jaenike, J., Unckless, R. L., Cockburn, S. N., Boelio, L. M. &Perlman, S. J. Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329, 212-215 (2010).
Cockburn, S. N. et al. Dynamics of the continent-wide spread of a Drosophila defensive symbiont. Ecol. Lett. 16, 609-616 (2013).
Xie, J., Vilchez, I. &Mateos, M. Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma. PLoS One 5, https://doi.org/10.1371/journal.pone.0012149 (2010).
Xie, J., Butler, S., Sanchez, G. &Mateos, M. Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps. Heredity 112, 399-408 (2014).
Fukatsu, T., Tsuchida, T., Nikoh, N. &Koga, R. Spiroplasma symbiont of the pea aphid, Acyrthosiphon pisum (Insecta: Homoptera). Appl. Environ. Microbiol. 67, 1284-1291 (2001).
Lukasik, P., Guo, H., van Asch, M., Ferrari, J. &Godfray, H. C. 2013. Protection against a fungal pathogen conferred by the aphid facultative endosymbionts Rickettsia and Spiroplasma is expressed in multiple host genotypes and species and is not influenced by co-infection with another symbiont. J. Evol. Biol. 26, 2654-2661 (2013).
Russell, J. A. et al. Uncovering symbiont-driven genetic diversity across North American pea aphids. Molec. Ecol. 22, 2045-2059 (2013).
Brady, C. M. et al. Worldwide populations of the aphid Aphis craccivora are infected with diverse facultative bacterial symbionts. Microb. Ecol. 67, 195-204 (2014).
Guidolin, A. S. &Cônsoli, F. L. Diversity of the most commonly reported facultative symbionts in two closely-related aphids with different host ranges. Neotr. Entomol. https://doi.org/10.1007/s13744-017-0532-0 (2017).
Halbert, S. E. &Brown, L. G. Brown Citrus Aphid, Toxoptera citricida (Kirkaldy) (Insecta: Hemiptera: Aphididae). Florida: University of Florida IFAS Extension (2011).
Guidolin, A. S. Multipartite interactions of Aphis (Toxoptera) and their associated symbionts. Thesis: Escola Superior de Agricultura "Luiz de Queiroz". available In, http://www.teses.usp.br/teses/disponiveis/11/11146/tde-26092016-095921/ (2016).
Feder, M. E. &Hofmann, G. E. Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and ecological physiology. Ann. Rev. Physiol. 61, 243-282 (1999).
Kaufmann, S. H. E. Heat-shock proteins and the immune-respose. Immunol. Today 11, 129-136 (1990).
King, A. M. &Macrae, T. H. Insect heat shock proteins during stress and diapause. Ann. Rev. Entomol. 60, 59-75 (2015).
Schlesinger, M. J. Heat-shock proteins. J. Biol. Chem. 265, 12111-12114 (1990).
Otvos, L. O. I. Jr. et al. Interaction between heat shock proteins and antimicrobial peptides. Biochem. 39, 14150-14159 (2000).
Pockley, A. G. Heat shock proteins as regulators of the immune response. Lancet 362, 469-476 (2003).
Li, Y., Xiang, Q., Zhang, Q., Huang, Y. &Su, Z. Overview on the recent study of antimicrobial peptides: origins, functions, relative mechanisms and application. Peptides 37, 207-215 (2012).
Kragol, G. et al. The antibacterial peptide pyrrhocoricin inhibits the ATPase action of DnaK and prevents chaperone-assisted protein folding. Biochem. 40, 3016-3026 (2004).
Roy, R. N., Lomakin, I. B., Gagnon, M. G. &Steitz, T. A. The mechanism of inhibition of protein synthesis by the proline-rich peptide oncocin. Nat. Struct. Mol. Biol. 22, 466-469 (2015).
Taniguchi, M. et al. Pyrrhocoricin, a proline-rich antimicrobial peptide derived from insect, inhibits the translation process in the cell-free Escherichia coli protein synthesis system. J. Biosci. Bioeng. 121, 591-598 (2016).
Haft, D. H. &Basu, M. K. Biological systems discovery in silico: radical S-Adenosylmethionine protein families and their target peptides for posttranslational modification. J. Bacteriol. 193, 2745-2755 (2011).
Hansen, A. K. &Moran, N. A. Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. P. Natl. Acad. Sci. USA 108, 2849-2854 (2011).
Price, D. R. G. et al. Aphid amino acid transporter regulates glutamine supply to intracellular bacterial symbionts. P. Natl. Acad. Sci. USA 111, 320-325 (2014).
Russell, C. W. et al. Matching the supply of bacterial nutrients to the nutritional demand of the animal host. Proc. R. Soc. London-B 281, https://doi.org/10.1098/rspb.2014.1163 (2014).
Viola, R. E. The central enzymes of the aspartate family of amino acid biosynthesis. Acc. Chem. Res. 34, 339-349 (2001).
Dowling, D. K. &Simmons, L. W. Reactive oxygen species as universal constraints in life-history evolution. Proc. R. Soc. London-B 276, 1737-1745 (2009).
Wolf, D. H. &Hilt, W. The proteasome: a proteolytic nanomachine of cell regulation and waste disposal. Biochim. Biophys. Acta Molec. Cell Res. 1695, 19-31 (2004).
Kleiger, G. &Mayor, T. Perilous journey: a tour of the ubiquitin-proteasome system. Trends Cell Biol. 24, 352-359 (2014).