Environmental Factors and the Symbiont Cardinium Influence the Bacterial Microbiome of Spider Mites Across the Landscape.
Bacterial community
Cardinium
Microbiome
Spider mite
Tetranychus
Journal
Microbial ecology
ISSN: 1432-184X
Titre abrégé: Microb Ecol
Pays: United States
ID NLM: 7500663
Informations de publication
Date de publication:
22 Nov 2023
22 Nov 2023
Historique:
received:
10
08
2023
accepted:
30
10
2023
medline:
23
11
2023
pubmed:
22
11
2023
entrez:
22
11
2023
Statut:
epublish
Résumé
Microbes play a key role in the biology, ecology, and evolution of arthropods. Despite accumulating data on microbial communities in arthropods that feed on plants using piercing-sucking mouthparts, we still lack a comprehensive understanding of the composition and assembly factors of the microbiota, particularly in field-collected spider mites. Here, we applied 16S rRNA amplicon sequencing to investigate the characters of the bacterial community in 140 samples representing 420 mite individuals, belonging to eight Tetranychus species (Acari: Tetranychidae) collected from 26 sites in China. The results showed that the bacterial composition of spider mites varied significantly among different species, locations, and plants. The environment showed a significant influence on the bacterial community of spider mites, with different relative contributions. Latitude and precipitation were found to be the main factors influencing the bacterial community composition. The dissimilarity of bacterial community and geographical distance between mite locations were significantly correlated. The assembly of spider mite bacterial communities seemed to be mainly influenced by stochastic processes. Furthermore, the symbiont Cardinium was found to be important in shaping the microbiota of many Tetranychus species. The relative abundance of Cardinium was > 50% in T. viennensis, T. urticae G, T. urticae R, and T. turkestani. Removing Cardinium reads from our analysis significantly changed Shannon diversity index and weighted beta diversity in these species. Altogether, this study provides novel insights into bacterial diversity patterns that contribute to our knowledge of the symbiotic relationships between arthropods and their bacterial communities.
Identifiants
pubmed: 37991578
doi: 10.1007/s00248-023-02314-7
pii: 10.1007/s00248-023-02314-7
doi:
Substances chimiques
RNA, Ribosomal, 16S
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1Subventions
Organisme : National Natural Science Foundation of China
ID : 32001905 and 32020103011
Organisme : National Natural Science Foundation of China
ID : 32001905 and 32020103011
Organisme : National Key Research and Development Program of China
ID : 2022YFC2601000
Organisme : Natural Science Foundation of Jiangsu Province
ID : BK20211213
Organisme : Fundamental Research Funds for the Central Universities
ID : KJQN202110
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Stork NE (2018) How many species of insects and other terrestrial arthropods are there on earth? Annu Rev Entomol 63:31–45. https://doi.org/10.1146/annurev-ento-020117-043348
doi: 10.1146/annurev-ento-020117-043348
pubmed: 28938083
Wernegreen JJ (2012) Mutualism meltdown in insects: bacteria constrain thermal adaptation. Curr Opin Microbiol 15:255–262. https://doi.org/10.1016/j.mib.2012.02.001
doi: 10.1016/j.mib.2012.02.001
pubmed: 22381679
pmcid: 3590105
Bing X, Gerlach J, Loeb G, Buchon N (2018) Nutrient-dependent impact of microbes on Drosophila suzukii development. mBio 9:e02199-e2117. https://doi.org/10.1128/mBio.02199-17
doi: 10.1128/mBio.02199-17
pubmed: 29559576
pmcid: 5874910
Lax S, Cardona C, Zhao D, Winton VJ, Goodney G, Gao P, Gottel N, Hartmann EM, Henry C, Thomas PM, Kelley ST, Stephens B, Gilbert JA (2019) Microbial and metabolic succession on common building materials under high humidity conditions. Nat Commun 10:1767. https://doi.org/10.1038/s41467-019-09764-z
doi: 10.1038/s41467-019-09764-z
pubmed: 30992445
pmcid: 6467912
Zhu Y-X, Song Z-R, Huo S-M, Yang K, Hong X-Y (2020) Variation in the microbiome of the spider mite Tetranychus truncatus with sex, instar and endosymbiont infection. FEMS Microbiol Ecol 96:fiaa004. https://doi.org/10.1093/femsec/fiaa004
doi: 10.1093/femsec/fiaa004
pubmed: 31942975
Jones EW, Carlson JM, Sivak DA, Ludington WB (2022) Stochastic microbiome assembly depends on context. Proc Natl Acad Sci U S A 119:e2115877119. https://doi.org/10.1073/pnas.2115877119
doi: 10.1073/pnas.2115877119
pubmed: 35135881
pmcid: 8851475
Brinker P, Fontaine MC, Beukeboom LW, Falcao Salles J (2019) Host, symbionts, and the microbiome: the missing tripartite interaction. Trends Microbiol 27:480–488. https://doi.org/10.1016/j.tim.2019.02.002
doi: 10.1016/j.tim.2019.02.002
pubmed: 30857919
Duan X-Z, Sun J-T, Wang L-T, Shu X-H, Guo Y, Keiichiro M, Zhu Y-X, Bing X-L, Hoffmann AA, Hong X-Y (2020) Recent infection by Wolbachia alters microbial communities in wild Laodelphax striatellus populations. Microbiome 8:104. https://doi.org/10.1186/s40168-020-00878-x
doi: 10.1186/s40168-020-00878-x
pubmed: 32616041
pmcid: 7333401
Fromont C, Adair KL, Douglas AE (2019) Correlation and causation between the microbiome, Wolbachia and host functional traits in natural populations of drosophilid flies. Mol Ecol 28:1826–1841. https://doi.org/10.1111/mec.15041
doi: 10.1111/mec.15041
pubmed: 30714238
Dáder B, Then C, Berthelot E, Ducousso M, Ng JCK, Drucker M (2017) Insect transmission of plant viruses: multilayered interactions optimize viral propagation. Insect Sci 24:929–946. https://doi.org/10.1111/1744-7917.12470
doi: 10.1111/1744-7917.12470
pubmed: 28426155
Jing X, Wong ACN, Chaston JM, Colvin J, McKenzie CL, Douglas AE (2014) The bacterial communities in plant phloem-sap-feeding insects. Mol Ecol 23:1433–1444. https://doi.org/10.1111/mec.12637
doi: 10.1111/mec.12637
pubmed: 24350573
Wang D, Huang Z, He H, Wei C (2018) Comparative analysis of microbial communities associated with bacteriomes, reproductive organs and eggs of the cicada Subpsaltria yangi. Arch Microbiol 200:227–235. https://doi.org/10.1007/s00203-017-1432-8
doi: 10.1007/s00203-017-1432-8
pubmed: 28983672
Walter DE, Proctor HC (2013) Mites: ecology, evolution & behaviour. Springer, Dordrecht
doi: 10.1007/978-94-007-7164-2
Bensoussan N, Santamaria ME, Zhurov V, Diaz I, Grbić M, Grbić V (2016) Plant-herbivore interaction: dissection of the cellular pattern of Tetranychus urticae feeding on the host plant. Front Plant Sci 7. https://doi.org/10.3389/fpls.2016.01105
Hong X-Y (2011) Agricultural Acarology. China Agriculture Press Co., Ltd, Beijing
Leeuwen TV, Dermauw W (2016) The molecular evolution of xenobiotic metabolism and resistance in chelicerate mites. Annu Rev Entomol 61:475–498. https://doi.org/10.1146/annurev-ento-010715-023907
doi: 10.1146/annurev-ento-010715-023907
pubmed: 26982444
Zélé F, Santos I, Olivieri I, Weill M, Duron O, Magalhães S (2018) Endosymbiont diversity and prevalence in herbivorous spider mite populations in South-Western Europe. FEMS Microbiol Ecol 94. https://doi.org/10.1093/femsec/fiy015
Zhu Y-X, Song Y-L, Zhang Y-K, Hoffmann AA, Zhou J-C, Sun J-T, Hong X-Y (2018) Incidence of facultative bacterial endosymbionts in spider mites associated with local environment and host plant. Appl Environ Microbiol 84:e02546-e2517. https://doi.org/10.1128/aem.02546-17
doi: 10.1128/aem.02546-17
pubmed: 29330177
pmcid: 5835729
Zhang Y-K, Chen Y-T, Yang K, Qiao G-X, Hong X-Y (2016) Screening of spider mites (Acari: Tetranychidae) for reproductive endosymbionts reveals links between co-infection and evolutionary history. Sci Rep 6: 27900. https://doi.org/10.1038/srep27900 https://www.nature.com/articles/srep27900#supplementary-information
Chaisiri K, McGarry JW, Morand S, Makepeace BL (2015) Symbiosis in an overlooked microcosm: a systematic review of the bacterial flora of mites. Parasitology 142:1152–1162. https://doi.org/10.1017/S0031182015000530
doi: 10.1017/S0031182015000530
pubmed: 26004817
Zélé F, Weill M, Magalhães S (2018) Identification of spider-mite species and their endosymbionts using multiplex PCR. Exp Appl Acarol 74:123–138. https://doi.org/10.1007/s10493-018-0224-4
doi: 10.1007/s10493-018-0224-4
pubmed: 29435771
Xue W-X, Sun J-T, Witters J, Vandenhole M, Dermauw W, Bajda SA, Simma EA, Wybouw N, Villacis-Perez E, Van Leeuwen T (2023) Incomplete reproductive barriers and genomic differentiation impact the spread of resistance mutations between green- and red-colour morphs of a cosmopolitan mite pest. Mol Ecol 32:4278–4297. https://doi.org/10.1111/mec.16994
doi: 10.1111/mec.16994
pubmed: 37211626
Villacis-Perez E, Snoeck S, Kurlovs AH, Clark RM, Breeuwer JAJ, Van Leeuwen T (2021) Adaptive divergence and post-zygotic barriers to gene flow between sympatric populations of a herbivorous mite. Commun Biol 4:853. https://doi.org/10.1038/s42003-021-02380-y
doi: 10.1038/s42003-021-02380-y
pubmed: 34244609
pmcid: 8270941
Suh E, Sim C, Park J-J, Cho K (2015) Inter-population variation for Wolbachia induced reproductive incompatibility in the haplodiploid mite Tetranychus urticae. Exp Appl Acarol 65:55–71. https://doi.org/10.1007/s10493-014-9846-3
doi: 10.1007/s10493-014-9846-3
pubmed: 25091123
Gotoh T, Sugasawa J, Noda H, Kitashima Y (2007) Wolbachia-induced cytoplasmic incompatibility in Japanese populations of Tetranychus urticae (Acari: Tetranychidae). Exp Appl Acarol 42:1–16. https://doi.org/10.1007/s10493-007-9072-3
doi: 10.1007/s10493-007-9072-3
pubmed: 17447012
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 Mol Biol 29:193–204. https://doi.org/10.1111/imb.12620
doi: 10.1111/imb.12620
pubmed: 31596027
Wybouw N, Mortier F, Bonte D (2022) Interacting host modifier systems control Wolbachia-induced cytoplasmic incompatibility in a haplodiploid mite. Evolution Letters 6:255–265. https://doi.org/10.1002/evl3.282
doi: 10.1002/evl3.282
pubmed: 35784453
pmcid: 9233175
Zhao D-X, Zhang X-F, Hong X-Y (2013) Host-symbiont interactions in spider mite Tetranychus truncatus doubly infected with Wolbachia and Cardinium. Environ Entomol 42:445–452. https://doi.org/10.1603/EN12354
doi: 10.1603/EN12354
pubmed: 23726053
Zhu L-Y, Zhang K-J, Zhang Y-K, Ge C, Gotoh T, Hong X-Y (2012) Wolbachia strengthens Cardinium-induced cytoplasmic incompatibility in the spider mite Tetranychus piercei McGregor. Curr Microbiol 65:516–523. https://doi.org/10.1007/s00284-012-0190-8
doi: 10.1007/s00284-012-0190-8
pubmed: 22806335
Zhu Y-X, Song Z-R, Song Y-L, Hong X-Y (2020) Double infection of Wolbachia and Spiroplasma alters induced plant defense and spider mite fecundity. Pest Manag Sci 76:3273–3281. https://doi.org/10.1002/ps.5886
doi: 10.1002/ps.5886
pubmed: 32388920
Zhu Y-X, Song Z-R, Zhang Y-Y, Hoffmann AA, Hong X-Y (2021) Spider mites singly infected with either Wolbachia or Spiroplasma have reduced thermal tolerance. Front Microbiol 12. https://doi.org/10.3389/fmicb.2021.706321
Yang K, Chen H, Bing X-L, Xia X, Zhu Y-X, Hong X-Y (2021) Wolbachia and Spiroplasma could influence bacterial communities of the spider mite Tetranychus truncatus. Exp Appl Acarol 83:197–210. https://doi.org/10.1007/s10493-021-00589-4
doi: 10.1007/s10493-021-00589-4
pubmed: 33484388
Chen L, Sun J-T, Jin P-Y, Hoffmann AA, Bing X-L, Zhao D-S, Xue X-F, Hong X-Y (2020) Population genomic data in spider mites point to a role for local adaptation in shaping range shifts. Evol Appl 13:2821–2835. https://doi.org/10.1111/eva.13086
doi: 10.1111/eva.13086
pubmed: 33294025
pmcid: 7691463
Bing X-L, Zhao D-S, Peng C-W, Huang H-J, Hong X-Y (2020) Similarities and spatial variations of bacterial and fungal communities in field rice planthopper (Hemiptera: Delphacidae) populations. Insect Sci 27:947–963. https://doi.org/10.1111/1744-7917.12782
doi: 10.1111/1744-7917.12782
pubmed: 32198842
Zhu Y-X, Song Z-R, Song Y-L, Zhao D-S, Hong X-Y (2020) The microbiota in spider mite feces potentially reflects intestinal bacterial communities in the host. Insect Sci 27:859–868. https://doi.org/10.1111/1744-7917.12716
doi: 10.1111/1744-7917.12716
pubmed: 31411007
Ge C, Ding X-L, Zhang J-P, Hong X-Y (2013) Tetranychus urticae (green form) on Gossypium hirsutum in China: two records confirmed by aedeagus morphology and RFLP analysis. Syst Appl Acarol 18:239–244. https://doi.org/10.11158/saa.18.3.6
doi: 10.11158/saa.18.3.6
Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1–e1. https://doi.org/10.1093/nar/gks808
doi: 10.1093/nar/gks808
pubmed: 22933715
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu Y-X, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vázquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. https://doi.org/10.1038/s41587-019-0209-9
doi: 10.1038/s41587-019-0209-9
pubmed: 31341288
pmcid: 7015180
Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584. https://doi.org/10.7717/peerj.2584
doi: 10.7717/peerj.2584
pubmed: 27781170
pmcid: 5075697
Amir A, McDonald D, Navas-Molina JA, Kopylova E, Morton JT, Xu ZZ, Kightley EP, Thompson LR, Hyde ER, Gonzalez A, Knight R (2017) Deblur rapidly resolves single-nucleotide community sequence patterns. mSystems 2: https://doi.org/10.1128/msystems.00191-00116 . https://doi.org/10.1128/msystems.00191-16
Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Gregory Caporaso J (2018) Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome 6:90. https://doi.org/10.1186/s40168-018-0470-z
doi: 10.1186/s40168-018-0470-z
pubmed: 29773078
pmcid: 5956843
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219
doi: 10.1093/nar/gks1219
pubmed: 23193283
pmcid: 3531112
Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R (2011) UniFrac: an effective distance metric for microbial community comparison. ISME J 5:169–172. https://doi.org/10.1038/ismej.2010.133
doi: 10.1038/ismej.2010.133
pubmed: 20827291
Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests M (2007) The vegan package. Community Ecol Package 10:631–637
McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. Plos One 8:e61217. https://doi.org/10.1371/journal.pone.0061217
doi: 10.1371/journal.pone.0061217
pubmed: 23630581
pmcid: 3632530
R Team C (2022) R: a language and environment for statistical computing R Foundation for Statistical Computing. http://www.R-project.org/
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer
doi: 10.1007/978-3-319-24277-4
Sloan WT, Lunn M, Woodcock S, Head IM, Nee S, Curtis TP (2006) Quantifying the roles of immigration and chance in shaping prokaryote community structure. Environ Microbiol 8:732–740. https://doi.org/10.1111/j.1462-2920.2005.00956.x
doi: 10.1111/j.1462-2920.2005.00956.x
pubmed: 16584484
Stegen JC, Lin X, Fredrickson JK, Chen X, Kennedy DW, Murray CJ, Rockhold ML, Konopka A (2013) Quantifying community assembly processes and identifying features that impose them. ISME J 7:2069–2079. https://doi.org/10.1038/ismej.2013.93
doi: 10.1038/ismej.2013.93
pubmed: 23739053
pmcid: 3806266
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. https://doi.org/10.1093/bioinformatics/btq166
doi: 10.1093/bioinformatics/btq166
pubmed: 20395285
Auger P, Migeon A, Ueckermann EA, Tiedt L, Navajas M (2013) Evidence for synonymy between Tetranychus urticae and Tetranychus cinnabarinus (Acari, Prostigmata, Tetranychidae): Review and new data. Acarologia 53:383–415. https://doi.org/10.1051/acarologia/20132102
doi: 10.1051/acarologia/20132102
Jin P-Y, Tian L, Chen L (2012) Hong X-Y (2018) Spider mites of agricultural importance in China, with focus on species composition during the last decade (2008–2017). Syst Appl Acarol 23:2087–2098
Gawande SJ, Anandhan S, Ingle A, Roylawar P, Khandagale K, Gawai T, Jacobson A, Asokan R, Singh M (2019) Microbiome profiling of the onion thrips, Thrips tabaci Lindeman (Thysanoptera: Thripidae). Plos One 14:e0223281. https://doi.org/10.1371/journal.pone.0223281
doi: 10.1371/journal.pone.0223281
pubmed: 31568480
pmcid: 6768462
Baumann P (2005) Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59:155–189. https://doi.org/10.1146/annurev.micro.59.030804.121041
doi: 10.1146/annurev.micro.59.030804.121041
pubmed: 16153167
Lemoine R, La Camera S, Atanassova R, Dédaldéchamp F, Allario T, Pourtau N, Bonnemain J-L, Laloi M, Coutos-Thévenot P, Maurousset L, Faucher M, Girousse C, Lemonnier P, Parrilla J, Durand M (2013) Source-to-sink transport of sugar and regulation by environmental factors. Front Plant Sci 4. https://doi.org/10.3389/fpls.2013.00272
Näpflin K, Schmid-Hempel P (2018) Host effects on microbiota community assembly. J Anim Ecol 87:331–340. https://doi.org/10.1111/1365-2656.12768
doi: 10.1111/1365-2656.12768
pubmed: 29023693
Van Opijnen T, Breeuwer J (1999) High temperatures eliminate Wolbachia, a cytoplasmic incompatibility inducing endosymbiont, from the two-spotted spider mite. Exp Appl Acarol 23:871–881
doi: 10.1023/A:1006363604916
pubmed: 10668862
Sieber M, Pita L, Weiland-Bräuer N, Dirksen P, Wang J, Mortzfeld B, Franzenburg S, Schmitz RA, Baines JF, Fraune S, Hentschel U, Schulenburg H, Bosch TCG, Traulsen A (2019) Neutrality in the metaorganism. Plos Biol 17:e3000298. https://doi.org/10.1371/journal.pbio.3000298
doi: 10.1371/journal.pbio.3000298
pubmed: 31216282
pmcid: 6583948
Ge Y, Jing Z, Diao Q, He J-Z, Liu Y-J (2021) Host species and geography differentiate honeybee gut bacterial communities by changing the relative contribution of community assembly processes. mBio 12:e00751-00721. https://doi.org/10.1128/mBio.00751-21
doi: 10.1128/mBio.00751-21
pubmed: 34061602
pmcid: 8262996
Gottlieb Y, Ghanim M, Gueguen G, Kontsedalov S, Vavre F, Fleury F, Zchori-Fein E (2008) Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies. FASEB J 22:2591–2599. https://doi.org/10.1096/Fj.07-101162
doi: 10.1096/Fj.07-101162
pubmed: 18285399
Zchori-Fein E, Perlman SJ (2004) Distribution of the bacterial symbiont Cardinium in arthropods. Mol Ecol 13:2009–2016. https://doi.org/10.1046/j.1365-294X.2004.02203.x
doi: 10.1046/j.1365-294X.2004.02203.x
pubmed: 15189221
Hubert J, Nesvorna M, Klimov PB, Erban T, Sopko B, Dowd SE, Scully ED, Bordenstein S (2021) Interactions of the intracellular bacterium Cardinium with its host, the house dust mite Dermatophagoides farinae, based on gene expression data. mSystems 6:e00916-00921. https://doi.org/10.1128/mSystems.00916-21
doi: 10.1128/mSystems.00916-21
pubmed: 34726490
pmcid: 8562489
Zhang Y-K, Chen Y-T, Yang K, Hong X-Y (2016) A review of prevalence and phylogeny of the bacterial symbiont Cardinium in mites (subclass: Acari). Syst Appl Acarol 21:978–990. https://doi.org/10.11158/saa.21.7.11
doi: 10.11158/saa.21.7.11
Liu Y, Xie R-R, Hong X-Y (2010) Manipulation of symbiont Cardinium on the reproduction of the carmine spidermite, Tetranychus cinnabarinus (Boisduval) (Acari:Tetranychidae). Acta Entomol Sin 53:1233–1240
Gotoh T, Noda H, Ito S (2007) Cardinium symbionts cause cytoplasmic incompatibility in spider mites. Heredity 98:13–20. https://doi.org/10.1038/sj.hdy.6800881
doi: 10.1038/sj.hdy.6800881
pubmed: 17035954