Experimental Manipulation Shows a Greater Influence of Population than Dietary Perturbation on the Microbiome of Tyrophagus putrescentiae
Jazyk angličtina Země Spojené státy americké Médium electronic-print
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
28235879
PubMed Central
PMC5394330
DOI
10.1128/aem.00128-17
PII: AEM.00128-17
Knihovny.cz E-zdroje
- Klíčová slova
- 16S rRNA, Bartonella, Blattabacterium, Cardinium, Solitalea, Tyrophagus putrescentiae, Wolbachia, bacteria, feeding, fitness, symbiont,
- MeSH
- Acaridae mikrobiologie MeSH
- Bacteria klasifikace genetika MeSH
- dieta metody MeSH
- DNA bakterií chemie genetika MeSH
- kvantitativní polymerázová řetězová reakce MeSH
- ribozomální DNA chemie genetika MeSH
- RNA ribozomální 16S genetika MeSH
- sekvenční analýza DNA MeSH
- shluková analýza MeSH
- stravovací zvyklosti MeSH
- střevní mikroflóra * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- DNA bakterií MeSH
- ribozomální DNA MeSH
- RNA ribozomální 16S MeSH
Tyrophagus putrescentiae is inhabited by bacteria that differ among mite populations (strains) and diets. Here, we investigated how the microbiome and fitness of Tputrescentiae are altered by dietary perturbations and mite populations. Four T. putrescentiae populations, referred to as dog, Koppert, laboratory, and Phillips, underwent a perturbation, i.e., a dietary switch from a rearing diet to two experimental diets. The microbiome was investigated by sequencing the V1-V3 portion of the 16S rRNA gene, and selected bacterial taxa were quantified by quantitative PCR (qPCR) using group/taxon-specific primers. The parameters observed were the changes in mite population growth and nutritional status, i.e., the total glycogen, lipid, saccharide, and protein contents in mites. The effect of diet perturbation on the variability of the microbiome composition and population growth was lower than the effect induced by mite population. In contrast, the diet perturbation showed a greater effect on nutritional status of mites than the mite population. The endosymbionts exhibited high variations among T. putrescentiae populations, including Cardinium in the laboratory population, Blattabacterium-like bacteria in the dog population, and Wolbachia in the dog and Phillips populations. Solitalea-like and Bartonella-like bacteria were present in the dog, Koppert, and Phillips populations in different proportions. The T. putrescentiae microbiome is dynamic and varies based on both the mite population and perturbation; however, the mites remain characterized by robust bacterial communities. Bacterial endosymbionts were found in all populations but represented a dominant portion of the microbiome in only some populations.IMPORTANCE We addressed the question of whether population origin or perturbation exerts a more significant influence on the bacterial community of the stored product mite Tyrophagus putrescentiae The microbiomes of four populations of T. putrescentiae insects subjected to diet perturbation were compared. Based on our results, the bacterial community was more affected by the mite population than by diet perturbation. This result can be interpreted as indicating high stability of the putative intracellular symbionts in response to dietary perturbation. The changes in the absolute and relative numbers of Wolbachia, Blattabacterium-like, Solitalea-like, and Cardinium bacteria in the T. putrescentiae populations can also be caused by neutral processes other than perturbation. When nutritional status is considered, the effect of population appeared less important than the perturbation. We hypothesize that differences in the proportions of the endosymbiotic bacteria result in changes in mite population growth.
Zobrazit více v PubMed
Dale C, Moran NA. 2006. Molecular interactions between bacterial symbionts and their hosts. Cell 126:453–465. doi:10.1016/j.cell.2006.07.014. PubMed DOI
Feldhaar H. 2011. Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol 36:533–543. doi:10.1111/j.1365-2311.2011.01318.x. DOI
McLean AHC, Parker BJ, Hrcek J, Henry LM, Godfray HCJ. 2016. Insect symbionts in food webs. Philos Trans R Soc Lond B Biol Sci 371:20150325. doi:10.1098/rstb.2015.0325. PubMed DOI PMC
Ferrari J, Vavre F. 2011. Bacterial symbionts in insects or the story of communities affecting communities. Philos Trans R Soc Lond B Biol Sci 366:1389–1400. doi:10.1098/rstb.2010.0226. PubMed DOI PMC
Weinert LA, Araujo-Jnr EV, Ahmed MZ, Welch JJ. 2015. The incidence of bacterial endosymbionts in terrestrial arthropods. Proc Biol Sci 282:20150249. doi:10.1098/rspb.2015.0249. PubMed DOI PMC
Werren JH, Baldo L, Clark ME. 2008. Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751. doi:10.1038/nrmicro1969. PubMed DOI
Ros VID, Fleming VM, Feil EJ, Breeuwer JAJ. 2012. Diversity and recombination in Wolbachia and Cardinium from Bryobia spider mites. BMC Microbiol 12:S13. doi:10.1186/1471-2180-12-S1-S13. PubMed DOI PMC
Brown AN, Lloyd VK. 2015. Evidence for horizontal transfer of Wolbachia by a Drosophila mite. Exp Appl Acarol 66:301–311. doi:10.1007/s10493-015-9918-z. PubMed DOI
Hubert J, Kopecky J, Sagova-Mareckova M, Nesvorna M, Zurek L, Erban T. 2016. Assessment of bacterial communities in thirteen species of laboratory-cultured domestic mites (Acari: Acaridida). J Econ Entomol 109:1887–1896. doi:10.1093/jee/tow089. PubMed DOI
Hubert J, Kopecky J, Perotti MA, Nesvorna M, Braig HR, Sagova-Mareckova M, Macovei L, Zurek L. 2012. Detection and identification of species-specific bacteria associated with synanthropic mites. Microb Ecol 63:919–928. doi:10.1007/s00248-011-9969-6. PubMed DOI
Bowman CE. 1984. Comparative enzymology of economically important astigmatid mites, p 993–1001. In Griffiths DA, Bowman CE (ed), Acarology VI, vol 2 Ellis Horwood, Chichester, United Kingdom.
Childs M, Bowman CE. 1981. Lysozyme activity in six species of economically important astigmatid mites. Comp Biochem Physiol B Comp Biochem 70:615–617. doi:10.1016/0305-0491(81)90305-9. DOI
Bowman CE. 1981. Hide protease in stored product mites (Astigmata: Acaridae). Comp Biochem Physiol B Comp Biochem 70:803–805. doi:10.1016/0305-0491(81)90022-5. DOI
Rybanska D, Hubert J, Markovic M, Erban T. 2016. Dry dog food integrity and mite strain influence the density-dependent growth of the stored-product mite Tyrophagus putrescentiae (Acari: Acaridida). J Econ Entomol 109:454–460. doi:10.1093/jee/tov298. PubMed DOI
Erban T, Klimov PB, Smrz J, Phillips TW, Nesvorna M, Kopecky J, Hubert J. 2016. Populations of stored product mite Tyrophagus putrescentiae differ in their bacterial communities. Front Microbiol 7:1046. doi:10.3389/fmicb.2016.01046. PubMed DOI PMC
Hubert J, Kopecky J, Nesvorna M, Perotti MA, Erban T. 2016. Detection and localization of Solitalea-like and Cardinium bacteria in three Acarus siro populations (Astigmata: Acaridae). Exp Appl Acarol 70:309–327. doi:10.1007/s10493-016-0080-z. PubMed DOI
Smrz J. 2003. Microanatomical and biological aspects of bacterial associations in Tyrophagus putrescentiae (Acari: Acaridida). Exp Appl Acarol 31:105–113. doi:10.1023/B:APPA.0000005111.05959.d6. PubMed DOI
Smrz J, Catska V. 2010. Mycophagous mites and their internal associated bacteria cooperate to digest chitin in soil. Symbiosis 52:33–40. doi:10.1007/s13199-010-0099-6. DOI
Smrz J. 2006. Types of haemocytes in saprophagous soil mites (Acari: Oribatida, Acaridida), and the correlation between their presence and certain processes within mites. Eur J Entomol 103:679–686. doi:10.14411/eje.2006.088. DOI
Broderick NA, Raffa KF, Goodman RM, Handelsman J. 2004. Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl Environ Microbiol 70:293–300. doi:10.1128/AEM.70.1.293-300.2004. PubMed DOI PMC
Robinson CJ, Schloss P, Ramos Y, Raffa K, Handelsman J. 2010. Robustness of the bacterial community in the cabbage white butterfly larval midgut. Microb Ecol 59:199–211. doi:10.1007/s00248-009-9595-8. PubMed DOI PMC
Colman DR, Toolson EC, Takacs-Vesbach CD. 2012. Do diet and taxonomy influence insect gut bacterial communities? Mol Ecol 21:5124–5137. doi:10.1111/j.1365-294X.2012.05752.x. PubMed DOI
Yun J-H, Roh SW, Whon TW, Jung M-J, Kim M-S, Park D-S, Yoon C, Nam Y-D, Kim Y-J, Choi J-H, Kim J-Y, Shin N-R, Kim S-H, Lee W-J, Bae J-W. 2014. Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Appl Environ Microbiol 80:5254–5264. doi:10.1128/AEM.01226-14. PubMed DOI PMC
Erban T, Rybanska D, Hubert J. 2015. Population growth of the generalist mite Tyrophagus putrescentiae (Acari: Acaridida) following adaptation to high- or low-fat and high- or low-protein diets and the effect of dietary switch. Environ Entomol 44:1599–1604. doi:10.1093/ee/nvv129. PubMed DOI
Burns AR, Stephens WZ, Stagaman K, Wong S, Rawls JF, Guillemin K, Bohannan BJM. 2016. Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development. ISME J 10:655–664. doi:10.1038/ismej.2015.142. PubMed DOI PMC
Smrz J, Soukalova H, Catska V, Hubert J. 2016. Feeding patterns of Tyrophagus putrescentiae (Sarcoptiformes: Acaridae) indicate that mycophagy is not a single and homogeneous category of nutritional biology. J Insect Sci 16:94. doi:10.1093/jisesa/iew070. PubMed DOI PMC
Estes AM, Hearn DJ, Bronstein JL, Pierson EA. 2009. The olive fly endosymbiont, “Candidatus Erwinia dacicola,” switches from an intracellular existence to an extracellular existence during host insect development. Appl Environ Microbiol 75:7097–7106. doi:10.1128/AEM.00778-09. PubMed DOI PMC
Moran NA, Russell JA, Koga R, Fukatsu T. 2005. Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Appl Environ Microbiol 71:3302–3310. doi:10.1128/AEM.71.6.3302-3310.2005. PubMed DOI PMC
Behar A, Yuval B, Jurkevitch E. 2008. Gut bacterial communities in the Mediterranean fruit fly (Ceratitis capitata) and their impact on host longevity. J Insect Physiol 54:1377–1383. doi:10.1016/j.jinsphys.2008.07.011. PubMed DOI
Clark RM, Zera AJ, Behmer ST. 2015. Nutritional physiology of life-history trade-offs: how food protein-carbohydrate content influences life-history traits in the wing-polymorphic cricket Gryllus firmus. J Exp Biol 218:298–308. doi:10.1242/jeb.112888. PubMed DOI
Lee KP. 2015. Dietary protein:carbohydrate balance is a critical modulator of lifespan and reproduction in Drosophila melanogaster: a test using a chemically defined diet. J Insect Physiol 75:12–19. doi:10.1016/j.jinsphys.2015.02.007. PubMed DOI
Schwarz RS, Moran NA, Evans JD. 2016. Early gut colonizers shape parasite susceptibility and microbiota composition in honey bee workers. Proc Natl Acad Sci U S A 113:9345–9350. doi:10.1073/pnas.1606631113. PubMed DOI PMC
Matsumoto K. 1965. Studies on environmental factors for breeding of grain mites VII. Relationship between reproduction of mites and kind of carbohydrates in the diet. Jpn J Sanit Zool 16:118–122. (In Japanese.)
Hughes AM. 1976. The mites of stored food and houses, 2nd ed Technical bulletin 9. Ministry of Agriculture, Fisheries and Food, London, United Kingdom.
Santo Domingo JW, Kaufman MG, Klug MJ, Holben WE, Harris D, Tiedje JM. 1998. Influence of diet on the structure and function of the bacterial hindgut community of crickets. Mol Ecol 7:761–767. doi:10.1046/j.1365-294x.1998.00390.x. DOI
Wong A-C, Dobson AJ, Douglas AE. 2014. Gut microbiota dictates the metabolic response of Drosophila to diet. J Exp Biol 217:1894–1901. doi:10.1242/jeb.101725. PubMed DOI PMC
Hubert J, Nesvorna M, Sagova-Mareckova M, Kopecky J. 2012. Shift of bacterial community in synanthropic mite Tyrophagus putrescentiae induced by Fusarium fungal diet. PLoS One 7:e48429. doi:10.1371/journal.pone.0048429. PubMed DOI PMC
Erban T, Rybanska D, Harant K, Hortova B, Hubert J. 2016. Feces derived allergens of Tyrophagus putrescentiae reared on dried dog food and evidence of the strong nutritional interaction between the mite and Bacillus cereus producing protease bacillolysins and exo-chitinases. Front Physiol 7:53. doi:10.3389/fphys.2016.00053. PubMed DOI PMC
Erban T, Hubert J. 2010. Comparative analyses of proteolytic activities in seven species of synanthropic acaridid mites. Arch Insect Biochem Physiol 75:187–206. doi:10.1002/arch.20388. PubMed DOI
Serbus LR, White PM, Silva JP, Rabe A, Teixeira L, Albertson R, Sullivan W. 2015. The impact of host diet on Wolbachia titer in Drosophila. PLoS Pathog 11:e1004777. doi:10.1371/journal.ppat.1004777. PubMed DOI PMC
Su Q, Xie W, Wang S, Wu Q, Liu B, Fang Y, Xu B, Zhang Y. 2014. The endosymbiont Hamiltonella increases the growth rate of its host Bemisia tabaci during periods of nutritional stress. PLoS One 9:e89002. doi:10.1371/journal.pone.0089002. PubMed DOI PMC
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. doi:10.1038/srep27900. PubMed DOI PMC
Ros VID, Breeuwer JAJ. 2009. The effects of, and interactions between, Cardinium and Wolbachia in the doubly infected spider mite Bryobia sarothamni. Heredity 102:413–422. doi:10.1038/hdy.2009.4. PubMed DOI
Zhao D-X, Zhang X-F, Hong X-Y. 2013. Host-symbiont interactions in spider mite Tetranychus truncates doubly infected with Wolbachia and Cardinium. Environ Entomol 42:445–452. doi:10.1603/EN12354. PubMed DOI
Erban T, Hubert J. 2008. Digestive function of lysozyme in synanthropic acaridid mites enables utilization of bacteria as a food source. Exp Appl Acarol 44:199–212. doi:10.1007/s10493-008-9138-x. PubMed DOI
Stara J, Stejskal V, Nesvorna M, Plachy J, Hubert J. 2011. Efficacy of selected pesticides against synanthropic mites under laboratory assay. Pest Manag Sci 67:446–457. doi:10.1002/ps.2083. PubMed DOI
Gentle JE. 2007. Matrix algebra: theory, computations, and applications in statistics. Springer, New York, NY.
Borcard D, Gillet F, Legendre P. 2011. Numerical ecology with R, 1st ed. Springer, New York, NY.
Legendre P, Legendre L. 2012. Numerical ecology, 3rd ed. Elsevier, Amsterdam, the Netherlands.
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H. 2016. vegan: community ecology package. R Foundation for Statistical Computing, Vienna, Austria: https://CRAN.R-project.org/package=vegan.
R Core Team. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria: https://www.R-project.org.
Kaufmann C. 2014. Determination of lipid, glycogen and sugars in mosquitoes. In Benedict M. (ed), MR4 methods in Anopheles research, 4th ed BEI Resources, Manassas, VA.
Chiodini RJ, Dowd SE, Chamberlin WM, Galandiuk S, Davis B, Glassing A. 2015. Microbial population differentials between mucosal and submucosal intestinal tissues in advanced Crohn's disease of the ileum. PLoS One 10:e0134382. doi:10.1371/journal.pone.0134382. PubMed DOI PMC
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi:10.1128/AEM.01541-09. PubMed DOI PMC
Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. 2013. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120. doi:10.1128/AEM.01043-13. PubMed DOI PMC
Edgar RC. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. doi:10.1038/nmeth.2604. PubMed DOI
Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM. 2014. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42:D633–D642. doi:10.1093/nar/gkt1244. PubMed DOI PMC
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. doi:10.1093/nar/25.17.3389. PubMed DOI PMC
Ondov BD, Bergman NH, Phillippy AM. 2011. Interactive metagenomic visualization in a Web browser. BMC Bioinformatics 12:385. doi:10.1186/1471-2105-12-385. PubMed DOI PMC
Hammer O, Harper DAT, Ryan PD. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9–18.
Anderson MJ, Walsh DCI. 2013. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecol Monogr 83:557–574. doi:10.1890/12-2010.1. DOI
Kutner MH, Nachtsheim CJ, Neter J, Li W. 2005. Applied linear statistical models, 5th ed. McGraw-Hill Irwin, Boston, MA.
Dray S, Legendre P, Blanchet G. 2013. packfor: Forward selection with permutation (Canoco p 46). R Project for Statistical Computing, Vienna, Austria.
Warnes GR, Bolker B, Bonebakker L, Gentleman R, Huber W, Liaw A, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz M, Venables B. 2016. gplots: various R programming tools for plotting data. R Project for Statistical Computing, Vienna, Austria: https://CRAN.R-project.org/package=gplots.
Anderson MJ, Ellingsen KE, McArdle BH. 2006. Multivariate dispersion as a measure of beta diversity. Ecol Lett 9:683–693. doi:10.1111/j.1461-0248.2006.00926.x. PubMed DOI
Clarke KR, Somerfield PJ, Gorley RN. 2008. Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage. J Exp Mar Biol Ecol 366:56–69. doi:10.1016/j.jembe.2008.07.009. DOI
Whitaker D, Christman M. 2014. clustsig: Significant Cluster Analysis. https://CRAN.R-project.org/package=clustsig. R Project for Statistical Computing, Vienna, Austria.
White JR, Nagarajan N, Pop M. 2009. Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol 5:e1000352. doi:10.1371/journal.pcbi.1000352. PubMed DOI PMC
Microbial Communities of Stored Product Mites: Variation by Species and Population
Population and Culture Age Influence the Microbiome Profiles of House Dust Mites
Bacterial community associated with worker honeybees (Apis mellifera) affected by European foulbrood