Till evolution do us part: The diversity of symbiotic associations across populations of Philaenus spittlebugs.


Journal

Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692

Informations de publication

Date de publication:
11 2023
Historique:
received: 09 10 2022
accepted: 15 07 2023
medline: 15 11 2023
pubmed: 1 8 2023
entrez: 1 8 2023
Statut: ppublish

Résumé

Symbiotic bacteria have played crucial roles in the evolution of sap-feeding insects and can strongly affect host function. However, their diversity and distribution within species are not well understood; we do not know to what extent environmental factors or associations with other species may affect microbial community profiles. We addressed this question in Philaenus spittlebugs by surveying both insect and bacterial marker gene amplicons across multiple host populations. Host mitochondrial sequence data confirmed morphology-based identification of six species and revealed two divergent clades of Philaenus spumarius. All of them hosted the primary symbiont Sulcia that was almost always accompanied by Sodalis. Interestingly, populations and individuals often differed in the presence of Sodalis sequence variants, suggestive of intra-genome 16S rRNA variant polymorphism combined with rapid genome evolution and/or recent additional infections or replacements of the co-primary symbiont. The prevalence of facultative endosymbionts, including Wolbachia, Rickettsia, and Spiroplasma, varied among populations. Notably, cytochrome I oxidase (COI) amplicon data also showed that nearly a quarter of P. spumarius were infected by parasitoid flies (Verralia aucta). One of the Wolbachia operational taxonomic units (OTUs) was exclusively present in Verralia-parasitized specimens, suggestive of parasitoids as their source and highlighting the utility of host gene amplicon sequencing in microbiome studies.

Identifiants

pubmed: 37525959
doi: 10.1111/1462-2920.16473
doi:

Substances chimiques

RNA, Ribosomal, 16S 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2431-2446

Informations de copyright

© 2023 The Authors. Environmental Microbiology published by Applied Microbiology International and John Wiley & Sons Ltd.

Références

Ahmed, M.Z., Li, S.-J., Xue, X., Yin, X.-J., Ren, S.-X., Jiggins, F.M. et al. (2015) The intracellular bacterium Wolbachia uses parasitoid wasps as Phoretic vectors for efficient horizontal transmission. PLoS Pathogens, 11, e1004672.
Amiri, N., Keady, M.M. & Lim, H.C. (2023) Honey bees and bumble bees occupying the same landscape have distinct gut microbiomes and amplicon sequence variant-level responses to infections. PeerJ, 11, e15501.
Apprill, A., McNally, S., Parsons, R. & Weber, L. (2015) Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquatic Microbial Ecology, 75, 129-137.
Baldo, L., Dunning Hotopp, J.C., Jolley, K.A., Bordenstein, S.R., Biber, S.A., Choudhury, R.R. et al. (2006) Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Applied and Environmental Microbiology, 72, 7098-7110.
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, 112, 10169-10176.
Brumin, M., Kontsedalov, S. & Ghanim, M. (2011) Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Sci., 18, 57-66.
Buchner, P. (1965) Endosymbiosis of animals with plant microorganisms. New York: Interscience Publishers.
Douglas, A.E. (2009) The microbial dimension in insect nutritional ecology. Functional Ecology, 23, 38-47.
Douglas, A.E. (2016) How multi-partner endosymbioses function. Nature Reviews. Microbiology, 14, 731-743.
Driscoll, T.P., Verhoeve, V.I., Guillotte, M.L., Lehman, S.S., Rennoll, S.A., Beier-Sexton, M. et al. (2017) Wholly rickettsia! Reconstructed metabolic profile of the quintessential bacterial parasite of eukaryotic cells. MBio, 8, e00859-17.
Edgar, R.C. (2016) UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. bioRxiv, 081257.
Elbrecht, V., Braukmann, T.W.A., Ivanova, N.V., Prosser, S.W.J., Hajibabaei, M., Wright, M. et al. (2019) Validation of COI metabarcoding primers for terrestrial arthropods. PeerJ, 7, e7745.
Feldhaar, H. (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecological Entomology, 36, 533-543.
Formisano, G., Iodice, L., Cascone, P., Sacco, A., Quarto, R., Cavalieri, V. et al. (2022) Wolbachia infection and genetic diversity of Italian populations of Philaenus spumarius, the main vector of Xylella fastidiosa in Europe. PLoS One, 17, e0272028.
Fredensborg, B.L., Fossdal í Kálvalíð, I., Johannesen, T.B., Stensvold, C.R., Nielsen, H.V. & Kapel, C.M. (2020) Parasites modulate the gut-microbiome in insects: a proof-of-concept study. PLoS One, 15, e0227561.
Gerardo, N.M. & Parker, B.J. (2014) Mechanisms of symbiont-conferred protection against natural enemies: an ecological and evolutionary framework. Current Opinion in Insect Science, 4, 8-14.
Glenn, T.C. (2011) Field guide to next-generation DNA sequencers. Molecular Ecology Resources, 11, 759-769.
Godefroid, M., Morente, M., Schartel, T., Cornara, D., Purcell, A., Gallego, D. et al. (2021) Climate tolerances of Philaenus spumarius should be considered in risk assessment of disease outbreaks related to Xylella fastidiosa. Journal of Pest Science, 95, 855-868.
Hague, M.T.J., Caldwell, C.N. & Cooper, B.S. (2020) Pervasive effects of Wolbachia on host temperature preference. MBio, 11, e01768-20.
Himler, A.G., Adachi-Hagimori, T., Bergen, J.E., Kozuch, A., Kelly, S.E., Tabashnik, B.E. et al. (2011) Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science, 332, 254-256.
Hrček, J. & Godfray, H.C.J. (2015) What do molecular methods bring to host-parasitoid food webs? Trends in Parasitology, 31, 30-35.
Hubert, J., Navratilova, B., Sopko, B., Nesvorna, M. & Phillips, T.W. (2022) Pesticide residue exposure provides different responses of the microbiomes of distinct cultures of the stored product pest mite Acarus siro. BMC Microbiology, 22, 1-15.
Hunter, D.J., Torkelson, J.L., Bodnar, J., Mortazavi, B., Laurent, T., Deason, J. et al. (2015) The Rickettsia endosymbiont of Ixodes pacificus contains all the genes of De novo folate biosynthesis. PLoS One, 10, e0144552.
Husnik, F. & McCutcheon, J.P. (2016) Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis. PNAS, 113, E5416-E5424.
Jaenike, J., Unckless, R., Cockburn, S.N., Boelio, L.M. & Perlman, S.J. (2010) Adaptation via Symbiosis: recent spread of a drosophila defensive symbiont. Science, 329, 212-215.
Ju, J.-F., Bing, X.-L., Zhao, D.-S., Guo, Y., Xi, Z., Hoffmann, A. A. et al. (2019). Wolbachia supplement biotin and riboflavin to enhance reproduction in planthoppers. The ISME Journal, 14, 676-687.
Kapantaidaki, D.E., Antonatos, S., Evangelou, V., Papachristos, D.P. & Milonas, P. (2021) Genetic and endosymbiotic diversity of Greek populations of Philaenus spumarius, Philaenus signatus and Neophilaenus campestris, vectors of Xylella fastidiosa. Scientific Reports, 11, 3752.
Kircher, M., Heyn, P. & Kelso, J. (2011) Addressing challenges in the production and analysis of Illumina sequencing data. BMC Genomics, 12, 1-14.
Knight, R., Vrbanac, A., Taylor, B.C., Aksenov, A., Callewaert, C., Debelius, J. et al. (2018) Best practices for analysing microbiomes. Nature Reviews Microbiology, 16, 410-422.
Koga, R. & Moran, N.A. (2014) Swapping symbionts in spittlebugs: evolutionary replacement of a reduced genome symbiont. The ISME Journal, 8, 1237-1246.
Koga, R., Bennett, G.M., Cryan, J.R. & Moran, N.A. (2013) Evolutionary replacement of obligate symbionts in an ancient and diverse insect lineage. Environmental Microbiology, 15, 2073-2081.
Kriesner, P., Hoffmann, A.A., Lee, S.F., Turelli, M. & Weeks, A.R. (2013) Rapid sequential spread of two Wolbachia variants in Drosophila simulans. PLoS Pathogens, 9, e1003607.
Kwong, W.K., Medina, L.A., Koch, H., Sing, K.W., Soh, E.J.Y., Ascher, J.S. et al. (2017) Dynamic microbiome evolution in social bees. Science Advances, 3, e1600513.
Leigh, J.W. & Bryant, D. (2015) POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6, 1110-1116.
Leray, M., Ho, S.-L., Lin, I.-J. & Machida, R.J. (2018) MIDORI server: a webserver for taxonomic assignment of unknown metazoan mitochondrial-encoded sequences using a curated database. Bioinformatics, 34, 3753-3754.
Lis, A., Maryańska-Nadachowska, A. & Kajtoch, Ł. (2015) Relations of Wolbachia infection with Phylogeography of Philaenus spumarius (Hemiptera: Aphrophoridae) populations within and beyond the Carpathian contact zone. Microbial Ecology, 70, 509-521.
Lis, A., Maryańska-Nadachowska, A., Lachowska-Cierlik, D. & Kajtoch, Ł. (2014) The secondary contact zone of phylogenetic lineages of the Philaenus spumarius (Hemiptera: Aphrophoridae): an example of incomplete allopatric speciation. Journal of Insect Science, 14, 1-10.
Maejima, K., Oshima, K. & Namba, S. (2014) Exploring the phytoplasmas, plant pathogenic bacteria. Journal of General Plant Pathology, 80, 210-221.
Mansfield, J., Genin, S., Magori, S., Citovsky, V., Sriariyanum, M., Ronald, P. et al. (2012) Top 10 plant pathogenic bacteria in molecular plant pathology. Molecular Plant Pathology, 13, 614-629.
Martinson, V.G., Gawryluk, R.M.R., Gowen, B.E., Curtis, C.I., Jaenike, J. & Perlman, S.J. (2020) Multiple origins of obligate nematode and insect symbionts by a clade of bacteria closely related to plant pathogens. PNAS, 117, 31979-31986.
Maryańska-Nadachowska, A., Drosopoulos, S., Lachowska, D., Kajtoch, Ł. & Kuznetsova, V.G. (2010) Molecular phylogeny of the Mediterranean species of Philaenus (Hemiptera: Auchenorrhyncha: Aphrophoridae) using mitochondrial and nuclear DNA sequences. Systematic Entomology, 35, 318-328.
Maryańska-Nadachowska, A., Kajtoch, Ł. & Lachowska, D. (2012) Genetic diversity of Philaenus spumarius and P. tesselatus (Hemiptera, Aphrophoridae): implications for evolution and taxonomy. Systematic Entomology, 37, 55-64.
Maryańska-Nadachowska, A., Sanaieb, E. & Kajtocha, Ł. (2015) High genetic diversity in southwest Asian populations of Philaenus spumarius (Hemiptera: Auchenorrhyncha). Zoology in the Middle East, 61, 264-272.
McCutcheon, J.P., Boyd, B.M. & Dale, C. (2019) The life of an insect endosymbiont from the cradle to the grave. Current Biology, 29, R485-R495.
McCutcheon, J.P., McDonald, B.R. & Moran, N.A. (2009) Convergent evolution of metabolic roles in bacterial co-symbionts of insects. PNAS, 106, 15394-15399.
Michalik, A., Castillo Franco, D., Kobiałka, M., Szklarzewicz, T., Stroiński, A. & Łukasik, P. (2021) Alternative transmission patterns in independently acquired nutritional cosymbionts of Dictyopharidae planthoppers. mBio, 12, e01228-21.
Molinatto, G., Demichelis, S., Bodino, N., Giorgini, M., Mori, N. & Bosco, D. (2020) Biology and prevalence in northern Italy of Verrallia aucta (Diptera, Pipunculidae), a parasitoid of Philaenus spumarius (Hemiptera, Aphrophoridae), the Main vector of Xylella fastidiosa in Europe. Insects, 11, 607.
Montllor, C.B., Maxmen, A. & Purcell, A.H. (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecological Entomology, 27, 189-195.
Moran, N.A., McCutcheon, J.P. & Nakabachi, A. (2008) Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics, 42, 165-190.
Nadal-Jimenez, P., Siozios, S., Halliday, N., Cámara, M. & Hurst, G.D. (2022) Symbiopectobacterium purcellii, gen. Nov., sp. nov., isolated from the leafhopper Empoasca decipiens, Vol. 72. United Kingdom: International Journal of Systematic and Evolutionary Microbiology, 005440.
Paddock, K.J., Finke, D.L., Kim, K.S., Sappington, T.W. & Hibbard, B.E. (2022) Patterns of microbiome composition vary across spatial scales in a specialist insect. Frontiers in Microbiology, 13, 898744.
Parada, A.E., Needham, D.M. & Fuhrman, J.A. (2016) Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environmental Microbiology, 18, 1403-1414.
Perreau, J. & Moran, N.A. (2022) Genetic innovations in animal-microbe symbioses. Nature Reviews Genetics, 23, 23-39.
Pilgrim, J., Thongprem, P., Davison, H.R., Siozios, S., Baylis, M., Zakharov, E.V. et al. (2021) Torix Rickettsia are widespread in arthropods and reflect a neglected symbiosis. GigaScience, 10, giab021.
Prodan, A., Tremaroli, V., Brolin, H., Zwinderman, A.H., Nieuwdorp, M. & Levin, E. (2020) Comparing bioinformatic pipelines for microbial 16S rRNA amplicon sequencing. PLoS One, 15, e0227434.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P. et al. (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research, 41, D590-D596.
Rodrigues, A.S.B., Silva, S.E., Marabuto, E., Silva, D.N., Wilson, M.R., Thompson, V. et al. (2014) New mitochondrial and nuclear evidences support recent demographic expansion and an atypical phylogeographic pattern in the spittlebug Philaenus spumarius (Hemiptera, Aphrophoridae). PLoS One, 9, e98375.
Rognes, T., Flouri, T., Nichols, B., Quince, C. & Mahé, F. (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ, 4, e2584.
Salter, S.J., Cox, M.J., Turek, E.M., Calus, S.T., Cookson, W.O., Moffatt, M.F. et al. (2014) Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biology, 12, 87.
Saponari, M., Loconsole, G., Cornara, D., Yokomi, R.K., de Stradis, A., Boscia, D. et al. (2014) Infectivity and transmission of Xylella fastidiosa by Philaenus spumarius (Hemiptera: Aphrophoridae) in Apulia, Italy. Journal of Economic Entomology, 107, 1316-1319.
SAS Institute Inc. (2013) SAS® 9.4 statements: reference. Cary, NC: SAS Institute Inc.
Seabra, S.G., Rodrigues, A.S.B., Silva, S.E., Neto, A.C., Pina-Martins, F., Marabuto, E. et al. (2021) Population structure, adaptation and divergence of the meadow spittlebug, Philaenus spumarius (Hemiptera, Aphrophoridae), revealed by genomic and morphological data. PeerJ, 9, e11425.
Sicard, A., Zeilinger, A.R., Vanhove, M., Schartel, T.E., Beal, D.J., Daugherty, M.P. et al. (2018) Xylella fastidiosa: insights into an emerging plant pathogen. Annual Reviews., 56, 181-202.
Smith, A.H., O'Connor, M.P., Deal, B., Kotzer, C., Lee, A., Wagner, B. et al. (2021) Does getting defensive get you anywhere?-Seasonal balancing selection, temperature, and parasitoids shape real-world, protective endosymbiont dynamics in the pea aphid. Molecular Ecology, 30, 2449-2472.
Smith, A.H., Łukasik, P., O'Connor, M.P., Lee, A., Mayo, G., Drott, M.T. et al. (2015) Patterns, causes and consequences of defensive microbiome dynamics across multiple scales. Molecular Ecology, 24, 1135-1149.
Song, H., Buhay, J.E., Whiting, M.F. & Crandall, K.A. (2008) Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Sciences, 105, 13486-13491.
Sow, A., Brévault, T., Benoit, L., Chapuis, M.-P., Galan, M., Coeur d'acier, A. et al. (2019) Deciphering host-parasitoid interactions and parasitism rates of crop pests using DNA metabarcoding. Scientific Reports, 9, 3646.
Tinker, K.A. & Ottesen, E.A. (2021) Differences in gut microbiome composition between sympatric wild and allopatric laboratory populations of omnivorous cockroaches. Frontiers in Microbiology, 12, 703785.
Tláskal, V., Pylro, V.S., Žifčáková, L. & Baldrian, P. (2021) Ecological divergence within the enterobacterial genus Sodalis: from insect symbionts to inhabitants of decomposing deadwood. Frontiers in Microbiology, 12, 668644.
Truitt, A.M., Kapun, M., Kaur, R. & Miller, W.J. (2019) Wolbachia modifies thermal preference in Drosophila melanogaster. Environmental Microbiology, 21, 3259-3268.
Vorburger, C. & Perlman, S.J. (2018) The role of defensive symbionts in host-parasite coevolution. Biological Reviews, 93, 1747-1764.
Vorburger, C. (2022) Defensive symbionts and the evolution of parasitoid host specialization. Annual Review of Entomology, 67, 329-346.
Zhang, J., Kobert, K., Flouri, T. & Stamatakis, A. (2014) PEAR: a fast and accurate Illumina paired-end reAd mergeR. Bioinformatics, 30, 614-620.
Łukasik, P., Guo, H., van Asch, M., Ferrari, J. & Godfray, H.C.J. (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. Journal of Evolutionary Biology, 26, 2654-2661.
Łukasik, P., Newton, J.A., Sanders, J.G., Hu, Y., Moreau, C.S., Kronauer, D.J.C. et al. (2017) The structured diversity of specialized gut symbionts of the New World army ants. Molecular Ecology, 26, 3808-3825.
Łukasik, P., van Asch, M., Guo, H., Ferrari, J. & Godfray, H.C.J. (2013) Unrelated facultative endosymbionts protect aphids against a fungal pathogen. Ecology Letters, 16, 214-218.
Šigut, M., Kostovčík, M., Šigutová, H., Hulcr, J., Drozd, P. & Hrček, J. (2017) Performance of DNA metabarcoding, standard barcoding, and morphological approach in the identification of host-parasitoid interactions. PLoS One, 12, e0187803.
Štarhová Serbina, L., Gajski, D., Malenovský, I., Corretto, E., Schuler, H. & Dittmer, J. (2022) Wolbachia infection dynamics in a natural population of the pear psyllid Cacopsylla pyri (Hemiptera: Psylloidea) across its seasonal generations. Scientific Reports, 12, 16502.

Auteurs

Michał Kolasa (M)

Institute of Environmental Sciences, Faculty of Biology, Jagiellonian University, Krakow, Poland.
Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Krakow, Poland.

Łukasz Kajtoch (Ł)

Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Krakow, Poland.

Anna Michalik (A)

Department of Developmental Biology and Morphology of Invertebrates, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University, Krakow, Poland.

Anna Maryańska-Nadachowska (A)

Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Krakow, Poland.

Piotr Łukasik (P)

Institute of Environmental Sciences, Faculty of Biology, Jagiellonian University, Krakow, Poland.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C

Classifications MeSH