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Bacterial communities in predatory mites are associated with species and diet types

Abstract

The symbiotic bacterial communities of phytophagous arthropods are affected by host species and feeding habits, but such effects have been poorly studied in natural enemies. Here, we investigated the entire bacterial microbiome of two species of predatory mites, Neoseiulus californicus and Neoseiulus barkeri, feeding on three types of diets (artificial diet, pollen and their natural prey, the spider mite Tetranychus urticae) by high-throughput sequencing of the 16S rRNA gene. We found that the bacterial diversity of predatory mites feeding on artificial diet was significantly different from pollen and spider mite feeding groups in both N. californicus and N. barkeri, while bacterial diversity also differed strikingly between the two species even when feeding on the same artificial diet. This finding suggests that the bacterial community of predatory mites is determined by both species and diet. Alphaproteobacteria and Gammaproteobacteria were the two dominant bacterial classes in both predatory mite species, except for N. californicus feeding on artificial diet. The bacterium Bosea sp. was detected in all samples as the core microbial species in predatory mites. Additionally, we discuss whether Bradyrhizobiaceae and Rhodobacteraceae bacteria could be used as probiotics in the artificial diet of N. californicus for better mass rearing.

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References

  1. Asshauer KP, Wemheuer B, Daniel R, Meinicke P (2015) Tax4Fun: predicting functional profiles from metagenomic 16S rRNA data. Bioinformatics 31:2882–2884

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  2. Augustinos AA, Kyritsis GA, Papadopoulos NT, Abd-Alla AM, Cáceres C, Bourtzis K (2015) Exploitation of the medfly gut microbiota for the enhancement of sterile insect technique: use of Enterobacter sp. in larval diet-based probiotic applications. PLoS ONE 10(9):e0136459

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  3. Ben Ami E, Yuval B, Jurkevitch E (2010) Manipulation of the microbiota of mass-reared Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidae) improves sterile male sexual performance. ISME J 4:28–37

    PubMed  Article  Google Scholar 

  4. Biere A, Tack AJM (2013) Evolutionary adaptation in three-way interactions between plants, microbes and arthropods. Funct Ecol 27:646–660

    Article  Google Scholar 

  5. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  6. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley JS, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  7. Calvo FJ, Bolckmans K, Belda JE (2011) Control of Bemisia tabaci and Frankliniella occidentalis in cucumber by Amblyseius swirskii. BioControl 56:185–192

    Article  Google Scholar 

  8. Chandler SM, Wilkinson TL, Douglas AE (2008) Impact of plant nutrients on the relationship between a herbivorous insect and its symbiotic bacteria. Proc Biol Sci 275:565–570

    CAS  PubMed  Google Scholar 

  9. Chong RA, Moran NA (2018) Evolutionary loss and replacement of Buchnera, the obligate endosymbiont of aphids. ISME J 12:898–908

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  10. Chu CC, Spencer JL, Curzi MJ, Zavala JA, Seufferheld MJ (2013) Gut bacteria facilitate adaptation to crop rotation in the western corn rootworm. Proc Natl Acad Sci USA 110:11917–11922

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  11. Chung SH, Scully ED, Peiffer M, Geib SM, Rosa C, Hoover K, Felton GW (2017) Host plant species determines symbiotic bacterial community mediating suppression of plant defenses. Sci Rep 7:39690

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  12. De Cock M, Virgilio M, Vandamme P, Bourtzis K, De Meyer M, Willems A (2020) Comparative microbiomics of Tephritid frugivorous pests (Diptera: Tephritidae) from the field: a tale of high variability across and within species. Front Microbiol 11:1890

    PubMed  PubMed Central  Article  Google Scholar 

  13. Douglas AE (2015) Multiorganismal insects: diversity and function of resident microorganisms. Annu Rev Entomol 60:17–34

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  14. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    CAS  Article  PubMed  Google Scholar 

  15. Edgar RC, Flyvbjerg H (2015) Error filtering, pair assembly and error correction for next-generation sequencing reads. Bioinformatics 31:3476–3482

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  16. Feldhaar H, Straka J, Krischke M, Berthold K, Stoll S, Mueller MJ, Gross R (2007) Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia. BMC Biol 5:48

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  17. Hammer TJ, Le E, Moran N (2021) Thermal niches of specialized gut symbionts: the case of social bees. Proc Biol Sci 288:20201480

    PubMed  PubMed Central  Google Scholar 

  18. Jaenike J (2015) Heritable symbionts contribute to host plant adaptation. Funct Ecol 29:1371–1372

    Article  Google Scholar 

  19. Jones RT, Bressan A, Greenwell AM, Fierer N (2011) Bacterial communities of two parthenogenetic aphid species cocolonizing two host plants across the Hawaiian Islands. Appl Environ Microbiol 77:8345–8349

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  20. Kapritchkoff FM, Viotti AP, Alli RP, Zuccolo M, Pradella J, Maiorano AE, Miranda EA, Bonomi A (2006) Enzymatic recovery and purification of polyhydroxybutyrate produced by Ralstonia eutropha. J Biotechnol 122:453–462

    CAS  PubMed  Article  Google Scholar 

  21. Kolodny O, Callahan BJ, Douglas AE (2020) The role of the microbiome in host evolution. Philos Trans R Soc Lond, B Biol Sci 375:20190588

    Article  Google Scholar 

  22. Kudo R, Masuya H, Endoh R, Kikuchi T, Ikeda H (2019) Gut bacterial and fungal communities in ground-dwelling beetles are associated with host food habit and habitat. ISME J 13:676–685

    CAS  PubMed  Article  Google Scholar 

  23. Lesperance DNA, Broderick NA, McBain AJ (2020) Gut bacteria mediate nutrient availability in Drosophila diets. Appl Environ Microbiol 87:e01401-e1420

    PubMed  PubMed Central  Article  Google Scholar 

  24. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI (2008) Evolution of mammals and their gut microbes. Science 320:1647–1651

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  25. Liu J, Lv JL, Wang ED, Xu XN, Wang SS (2019) Effects of artificial diets supplemented with different nutrient sources on the biology of Neoseiulus californicus. Chinese J Appl Entomol 56:710–717

    Google Scholar 

  26. Lombogia CA, Tulung M, Posangi J, Tallei TE (2020) Bacterial composition, community structure, and diversity in Apis nigrocincta gut. Int J Microbiol 2020:6906921

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  27. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  28. Majumder R, Sutcliffe B, Adnan SM, Mainali B, Dominiak BC, Taylor PW, Chapman TA (2020) Artificial larval diet mediates the microbiome of Queensland fruit fly. Front Microbiol 11:576156

    PubMed  PubMed Central  Article  Google Scholar 

  29. Marcondes de Souza JA, Carareto Alves LM, de Mello VA, de Macedo Lemos EG (2014) The family Bradyrhizobiaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes. Springer, Berlin, Heidelberg, pp 135–154

    Chapter  Google Scholar 

  30. McMurtry JA, Croft BA (1997) Life-styles of phytoseiid mites and their role in biological control. Annu Rev Entomol 42:291–321

    CAS  PubMed  Article  Google Scholar 

  31. McMurtry JA, Moraes GJD, Sourassou NF (2013) Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Syst Appl Acarol 18:297–320

    Google Scholar 

  32. Nguyen DT, Vangansbeke D, De Clercq P (2015) Performance of four species of phytoseiid mites on artificial and natural diets. Biol Control 80:56–62

    Article  Google Scholar 

  33. Pekas A, Palevsky E, Sumner JC, Perotti MA, Nesvorna M, Hubert J (2017) Comparison of bacterial microbiota of the predatory mite Neoseiulus cucumeris (Acari: Phytoseiidae) and its factitious prey Tyrophagus putrescentiae (Acari: Acaridae). Sci Rep 7:2

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  34. Pujalte MJ, Lucena T, Ruvira MA, Arahal DR, Macián MC (2014) The family Rhodobacteraceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes. Springer, Berlin, Germany, pp 439–512

    Chapter  Google Scholar 

  35. R Core Team (2019) R: A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. URL https://www.r-project.org/.

  36. Rodriguez-Cruz FA, Janssen A, Pallini A, Duarte MVA, Pinto CMF, Venzon M (2017) Two predatory mite species as potential control agents of broad mites. BioControl 62:505–513

    CAS  Article  Google Scholar 

  37. Safronova VI, Kuznetsova IG, Sazanova AL, Kimeklis AK, Belimov AA, Andronov EE, Pinaev AG, Chizhevskaya EP, Pukhaev AR, Popov KP, Willems A, Tikhonovich IA (2015) Bosea vaviloviae sp nov., a new species of slow-growing rhizobia isolated from nodules of the relict species Vavilovia formosa (Stev.) Fed. Anton Leeuw Int J G 107:911–920

    CAS  Article  Google Scholar 

  38. Sazanova AL, Safronova VI, Kuznetsova IG, Karlov DS, Belimov AA, Andronov EE, Chirak ER, Popova JP, Verkhozina AV, Willems A, Tikhonovich IA (2019) Bosea caraganae sp. nov. a new species of slow-growing bacteria isolated from root nodules of the relict species Caragana jubata (Pall.) Poir. originating from Mongolia. Int J Syst Evol Microbiol 69:2687–2695

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  39. Shuttleworth LA, Khan MAM, Collins D, Osborne T, Reynolds OL (2020) Wild bacterial probiotics fed to larvae of mass-reared Queensland fruit fly Bactrocera tryoni (Froggatt) do not impact long-term survival, mate selection, or locomotor activity. Insect Sci 27:745–755

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  40. Shuttleworth LA, Khan MAM, Osborne T, Collins D, Srivastava M, Reynolds OL (2019) A walk on the wild side: gut bacteria fed to mass-reared larvae of Queensland fruit fly Bactrocera tryoni (Froggatt) influence development. BMC Biotechnol 19:95

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  41. Song ZW, Nguyen DT, Li DS, De Clercq P (2019) Continuous rearing of the predatory mite Neoseiulus californicus on an artificial diet. BioControl 64:125–137

    Article  Google Scholar 

  42. Tsuchida T, Koga R, Shibao H, Matsumoto T, Fukatsu T (2002) Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum. Mol Ecol 11:2123–2135

    CAS  PubMed  Article  Google Scholar 

  43. Wagner SM, Martinez AJ, Ruan YM, Kim KL, Lenhart PA, Dehnel AC, Oliver KM, White JA (2015) Facultative endosymbionts mediate dietary breadth in a polyphagous herbivore. Funct Ecol 29:1402–1410

    Article  Google Scholar 

  44. Wong SD, Rawls JF (2012) Intestinal microbiota composition in fishes is influenced by host ecology and environment. Mol Ecol 21:3100–3102

    PubMed  PubMed Central  Article  Google Scholar 

  45. Wu S, Zhang Z, Gao Y, Xu X, Lei Z (2016) Interactions between foliage- and soil-dwelling predatory mites and consequences for biological control of Frankliniella occidentalis. BioControl 61:717–727

    Article  Google Scholar 

  46. Wu S, He Z, Wang E, Xu X, Lei Z (2017) Application of Beauveria bassiana and Neoseiulus barkeri for improved control of Frankliniella occidentalis in greenhouse cucumber. Crop Prot 96:83–87

    Article  Google Scholar 

  47. Yao MY, Zhang HH, Cai PM, Gu XH, Wang D, Ji QG (2017) Enhanced fitness of a Bactrocera cucurbitae genetic sexing strain based on the addition of gut-isolated probiotics (Enterobacter spec.) to the larval diet. Entomol Exp Appl 162:197–203

    Article  Google Scholar 

  48. Zhang JW, Xuan CG, Lu CH, Guo S, Yu JF, Asif M, Jiang WJ, Zhou ZG, Luo ZQ, Zhang LQ (2019) AidB, a novel thermostable N-Acylhomoserine lactonase from the bacterium Bosea sp. Appl Environ Microbiol 85:e02065-e2119

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Zhu YX, Song YL, Hoffmann AA, Jin PY, Huo SM, Hong XY (2019) A change in the bacterial community of spider mites decreases fecundity on multiple host plants. MicrobiologyOpen 8:e743

    Article  CAS  Google Scholar 

  50. Zhu YX, Song YL, Zhang YK, Hoffmann AA, Zhou JC, Sun JT, Hong XY (2018) Incidence of facultative bacterial endosymbionts in spider mites associated with local environments and host plants. Appl Environ Microbiol 84:e02546-e2617

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We appreciate Dr. Tobin Hammer for comments and editing. This research was supported by the National Natural Science Foundation of China (Grant No. 32070402) and Agricultural Science and Technology Innovation Program, CAAS “Protection and Application of Insect Natural Enemies”.

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JY, BZ and XX designed research; JY, BZ performed research; JY and BZ analyzed data; and JY, BZ, GL and XX wrote manuscript.

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Correspondence to Bo Zhang, Guiting Li or Xuenong Xu.

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On behalf of all authors, the corresponding author states that there is no conflict of interest.

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There are no ethical concerns regarding the organisms and the topic of this research.

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Handling Editor: Eric Riddick.

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Yan, J., Zhang, B., Li, G. et al. Bacterial communities in predatory mites are associated with species and diet types. BioControl (2021). https://doi.org/10.1007/s10526-021-10112-8

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Keywords

  • Microbiota
  • 16S rRNA
  • Neoseiulus
  • Feeding habit
  • Artificial diet
  • Probiotics