Variation of bacterial community assembly over developmental stages and midgut of Dermanyssus gallinae
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
205/2018
Programa Nacional de Becas de Postgrado en el Exterior "Don Carlos Antonio López"
SGCE - RAPPORT N° 0300
Collectivité de Corse
ANR-10-LABX-62-IBEID
Agence Nationale de la Recherche
22-18424M and 22-12648J
Grantová Agentura České Republiky
PubMed
37249591
DOI
10.1007/s00248-023-02244-4
PII: 10.1007/s00248-023-02244-4
Knihovny.cz E-zdroje
- Klíčová slova
- Dermanyssus gallinae, Functional prediction, Keystone taxa, Microbial networks, Microbiome,
- MeSH
- Bacteria genetika MeSH
- infestace roztoči * parazitologie prevence a kontrola MeSH
- kur domácí parazitologie MeSH
- nemoci drůbeže * parazitologie prevence a kontrola MeSH
- roztoči * mikrobiologie MeSH
- stadia vývoje MeSH
- zvířata MeSH
- Check Tag
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Bacterial microbiota play an important role in the fitness of arthropods, but the bacterial microflora in the parasitic mite Dermanyssus gallinae is only partially explored; there are gaps in our understanding of the microbiota localization and in our knowledge of microbial community assembly. In this work, we have visualized, quantified the abundance, and determined the diversity of bacterial occupancy, not only across developmental stages of D. gallinae, but also in the midgut of micro-dissected female D. gallinae mites. We explored community assembly and the presence of keystone taxa, as well as predicted metabolic functions in the microbiome of the mite. The diversity of the microbiota and the complexity of co-occurrence networks decreased with the progression of the life cycle. However, several bacterial taxa were present in all samples examined, indicating a core symbiotic consortium of bacteria. The relatively higher bacterial abundance in adult females, specifically in their midguts, implicates a function linked to the biology of D. gallinae mites. If such an association proves to be important, the bacterial microflora qualifies itself as an acaricidal or vaccine target against this troublesome pest.
EA 7310 Laboratoire de Virologie Université de Corse Corte France
INRAE UR 0045 Laboratoire de Recherches Sur Le Développement de L'Elevage 20250 Corte France
School of Environmental Sciences University of Guelph Guelph ON N1G 2W1 Canada
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Jiménez-Cortés JG, García-Contreras R, Bucio-Torres MI et al (2018) Bacterial symbionts in human blood-feeding arthropods: patterns, general mechanisms and effects of global ecological changes. Acta Trop 186:69–101. https://doi.org/10.1016/J.ACTATROPICA.2018.07.005 PubMed DOI
Douglas AE (2015) Multiorganismal insects: diversity and function of resident microorganisms. Annu Rev Entomol 60:17–34. https://doi.org/10.1146/ANNUREV-ENTO-010814-020822 PubMed DOI
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(1569):1389–1400. https://doi.org/10.1098/RSTB.2010.0226 PubMed DOI PMC
Sigognault Flochlay A, Thomas E, Sparagano O (2017) Poultry red mite (Dermanyssus gallinae) infestation: a broad impact parasitological disease that still remains a significant challenge for the egg-laying industry in Europe. Parasit Vectors 10:1–6. https://doi.org/10.1186/S13071-017-2292-4/FIGURES/1 DOI
Pritchard J, Kuster T, Sparagano O, Tomley F (2015) Understanding the biology and control of the poultry red mite Dermanyssus gallinae: a review. Avian Pathol 44(3):143–153. https://doi.org/10.1080/03079457.2015.1030589 PubMed DOI
Chauve C (1998) The poultry red mite Dermanyssus gallinae (De Geer, 1778): current situation and future prospects for control. Vet Parasitol 79:239–245. https://doi.org/10.1016/S0304-4017(98)00167-8 PubMed DOI
Price DRG, Bartley K, Blake DP et al (2021) A Rickettsiella endosymbiont is a potential source of essential B-vitamins for the poultry red mite, Dermanyssus gallinae. Front Microbiol 12:695346. https://doi.org/10.3389/FMICB.2021.695346/BIBTEX PubMed DOI PMC
Di Palma A, Giangaspero A, Cafiero MA, Germinara GS (2012) A gallery of the key characters to ease identification of Dermanyssus gallinae (Acari: Gamasida: Dermanyssidae) and allow differentiation from Ornithonyssus sylviarum (Acari: Gamasida: Macronyssidae). Parasit Vectors 5:1–10. https://doi.org/10.1186/1756-3305-5-104/FIGURES/8 DOI
Wang M, Zhu D, Dai J, Zhong Z, Zhang Y, Wang J (2018) Tissue localization and variation of major symbionts in Haemaphysalis longicornis, Rhipicephalus haemaphysaloides, and Dermacentor silvarum in China. Appl Environ Microbiol 84(10):e00029-18. https://doi.org/10.1128/AEM.00029-18 PubMed DOI PMC
Nadkarni MA, Martin FE, Jacques NA, Hunter N (2002) Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148(Pt 1):257–266. https://doi.org/10.1099/00221287-148-1-257 PubMed DOI
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29:e45–e45. https://doi.org/10.1093/NAR/29.9.E45 PubMed DOI PMC
Guizzo MG, Neupane S, Kucera M et al (2020) Poor unstable midgut microbiome of hard ticks contrasts with abundant and stable monospecific microbiome in ovaries. Front Cell Infect Microbiol 10:211. https://doi.org/10.3389/fcimb.2020.00211 PubMed DOI PMC
Parada AE, Needham DM, Fuhrman JA (2016) Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol 18:1403–1414. https://doi.org/10.1111/1462-2920.13023 PubMed DOI
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. Aquat Microb Ecol 75:129–137. https://doi.org/10.3354/AME01753 DOI
Davis NM, DiM P, Holmes SP, Relman DA, Callahan BJ (2018) Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome 6:226. https://doi.org/10.1186/s40168-018-0605-2 PubMed DOI PMC
Bolyen E, Rideout JR, Dillon MR et al (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 PubMed DOI PMC
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869 PubMed DOI PMC
Bokulich NA, Kaehler BD, Rideout JR et al (2018) Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome 6(1):90. https://doi.org/10.1186/s40168-018-0470-z PubMed DOI PMC
Yarza P, Yilmaz P, Pruesse E et al (2014) Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12(9):635–645. https://doi.org/10.1038/nrmicro3330 PubMed DOI
Friedman J, Alm EJ (2012) Inferring correlation networks from genomic survey data. PLoS Comput Biol 8(9):e1002687. https://doi.org/10.1371/journal.pcbi.1002687 PubMed DOI PMC
RStudio Team (2020) RStudio: integrated development for R. RStudio, PBC, Boston, MA URL http://www.rstudio.com/
Bastian M, Heymann S, Jacomy M (2009) Gephi : an open source software for exploring and manipulating networks visualization and exploration of large graphs. Third Int AAAI Conf Weblogs Soc Media. 3(1). https://doi.org/10.1609/icwsm.v3i1.13937
Ruhnau B (2000) Eigenvector-centrality—a node-centrality? Soc Networks 22:357–365. https://doi.org/10.1016/S0378-8733(00)00031-9 DOI
Peschel S, Müller CL, Von Mutius E, Boulesteix AL, Depner M (2021) NetCoMi: network construction and comparison for microbiome data in R. Brief Bioinform 22(4):bbaa290. https://doi.org/10.1093/BIB/BBAA290 PubMed DOI
Douglas GM, Maffei VJ, Zaneveld JR et al (2020) PICRUSt2 for prediction of metagenome functions. Nat Biotechnol 38:685–688. https://doi.org/10.1038/s41587-020-0548-6 PubMed DOI PMC
Kanehisa M, Goto S (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28(1):27–30. https://doi.org/10.1093/nar/28.1.27 PubMed DOI PMC
Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28(1):33–36. https://doi.org/10.1093/nar/28.1.33 PubMed DOI PMC
Caspi R, Billington R, Fulcher CA et al (2018) The MetaCyc database of metabolic pathways and enzymes. Nucleic Acids Res 48(D1):D445–D453. https://doi.org/10.1093/nar/gkx935 DOI
Fernandes AD, Reid JN, Macklaim JM, McMurrough TA, Edgell DR, Gloor GB (2014) Unifying the analysis of high-throughput sequencing datasets: characterizing RNA-seq, 16S rRNA gene sequencing and selective growth experiments by compositional data analysis. Microbiome 2:15. https://doi.org/10.1186/2049-2618-2-15 PubMed DOI PMC
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):550. https://doi.org/10.1186/S13059-014-0550-8/FIGURES/9 PubMed DOI PMC
Serrato-Salas J, Gendrin M (2022) Involvement of microbiota in insect physiology: focus on B vitamins. MBio. https://doi.org/10.1128/MBIO.02225-22 PubMed DOI PMC
Ross BD, Hayes B, Radey MC et al (2018) Ixodes scapularis does not harbor a stable midgut microbiome. ISME J 12(11):2596–2607. https://doi.org/10.1038/s41396-018-0161-6 PubMed DOI PMC
Hubert J, Erban T, Kopecky J et al (2017) Comparison of microbiomes between red poultry mite populations (Dermanyssus gallinae): predominance of Bartonella-like Bacteria. Microb Ecol 74(4):947–960. https://doi.org/10.1007/S00248-017-0993-Z PubMed DOI
Nishide Y, Sugimoto TN, Watanabe K, Egami H, Kageyama D (2022) Genetic variations and microbiome of the poultry red mite Dermanyssus gallinae. Front Microbiol 13:4315. https://doi.org/10.3389/FMICB.2022.1031535/BIBTEX DOI
Zhang R, Yu G, Huang Z, Zhang Z (2020) Microbiota assessment across different developmental stages of Dermacentor silvarum (Acari: Ixodidae) revealed stage-specific signatures. Ticks Tick Borne Dis 11(2):101321. https://doi.org/10.1016/j.ttbdis.2019.101321 PubMed DOI
Kwan JY, Griggs R, Chicana B, Miller C, Swei A (2017) Vertical vs. horizontal transmission of the microbiome in a key disease vector, Ixodes pacificus. Mol Ecol 26(23):6578–6589. https://doi.org/10.1111/mec.14391 PubMed DOI
Chicana B, Couper LI, Kwan JY, Tahiraj E, Swei A (2019) Comparative microbiome profiles of sympatric tick species from the far-western United States. Insects 10(10):353. https://doi.org/10.3390/insects10100353 PubMed DOI PMC
Zhang ZY, Ali MW, Saqib HSA et al (2020) A shift pattern of bacterial communities across the life stages of the citrus red mite, Panonychus citri. Front Microbiol 11:1620. https://doi.org/10.3389/FMICB.2020.01620 PubMed DOI PMC
Menchaca AC, Visi DK, Strey OF et al (2013) Preliminary assessment of microbiome changes following blood-feeding and survivorship in the Amblyomma americanum nymph-to-adult transition using semiconductor sequencing. PLoS One 8(6):e67129. https://doi.org/10.1371/journal.pone.0067129 PubMed DOI PMC
Swei A, Kwan JY (2017) Tick microbiome and pathogen acquisition altered by host blood meal. ISME J 11(3):813–816. https://doi.org/10.1038/ismej.2016.152 PubMed DOI
Wu-Chuang A, Hodžić A, Mateos-Hernández L, Estrada-Peña A, Obregon D, Cabezas-Cruz A (2021) Current debates and advances in tick microbiome research. Curr Res Parasitol Vector-Borne Dis 100036. https://doi.org/10.1016/j.crpvbd.2021.100036
de Almeida Lins K, Drummond MR, Velho PENF (2019) Cutaneous manifestations of bartonellosis. An Bras Dermatol 94(5):594–602. https://doi.org/10.1016/J.ABD.2019.09.024 DOI
George DR, Finn RD, Graham KM et al (2015) Should the poultry red mite Dermanyssus gallinae be of wider concern for veterinary and medical science? Parasit Vectors 8:1–10. https://doi.org/10.1186/S13071-015-0768-7/FIGURES/3 DOI
Valiente Moro C, Thioulouse J, Chauve C, Normand P, Zenner L (2009) Bacterial taxa associated with the hematophagous mite Dermanyssus gallinae detected by 16S rRNA PCR amplification and TTGE fingerprinting. Res Microbiol 160:63–70. https://doi.org/10.1016/J.RESMIC.2008.10.006 DOI
Valiente Moro C, De Luna CJ, Tod A, Guy JH, Sparagano OAE, Zenner L (2009) The poultry red mite (Dermanyssus gallinae): a potential vector of pathogenic agents. Exp Appl Acarol 48(1–2):93–104. https://doi.org/10.1007/S10493-009-9248-0 DOI
Schiavone A, Pugliese N, Otranto D et al (2022) Dermanyssus gallinae: the long journey of the poultry red mite to become a vector. Parasit Vectors 15:1–8. https://doi.org/10.1186/S13071-021-05142-1/TABLES/1 DOI
Röttjers L, Faust K (2018) From hairballs to hypotheses–biological insights from microbial networks. FEMS Microbiol Rev 42(6):761–780. https://doi.org/10.1093/FEMSRE/FUY030 PubMed DOI PMC
Berry D, Widder S (2014) Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front Microbiol 5:219. https://doi.org/10.3389/fmicb.2014.00219 PubMed DOI PMC
Mateos-Hernández L, Obregón D, Maye J et al (2020) Anti-tick microbiota vaccine impacts Ixodes ricinus performance during feeding. Vaccines 8(4):702. https://doi.org/10.3390/vaccines8040702 PubMed DOI PMC
Mateos-Hernández L, Obregón D, Wu-Chuang A et al (2021) Anti-microbiota vaccines modulate the tick microbiome in a taxon-specific manner. Front Immunol 12:704621. https://doi.org/10.3389/FIMMU.2021.704621 PubMed DOI PMC
Maitre A, Wu-Chuang A, Mateos-Hernández L et al (2022) Rickettsia helvetica infection is associated with microbiome modulation in Ixodes ricinus collected from humans in Serbia. Sci Reports 12(1):11464. https://doi.org/10.1038/s41598-022-15681-x DOI
Gomard Y, Flores O, Vittecoq M et al (2021) Changes in bacterial diversity, composition and interactions during the development of the seabird tick Ornithodoros maritimus (Argasidae). Microb Ecol 81(3):770–783. https://doi.org/10.1007/S00248-020-01611-9 PubMed DOI
Aželytė J, Wu-Chuang A, Žiegytė R et al (2022) Anti-microbiota vaccine reduces avian malaria infection within mosquito vectors. Front Immunol 13:841835. https://doi.org/10.3389/FIMMU.2022.841835/BIBTEX PubMed DOI PMC
Banerjee S, Schlaeppi K, van der Heijden MGA (2018) Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol 16(9):567–576. https://doi.org/10.1038/s41579-018-0024-1 PubMed DOI
Wu-Chuang A, Obregon D, Estrada-Peña A, Cabezas-Cruz A (2021) Thermostable keystone bacteria maintain the functional diversity of the Ixodes scapularis microbiome under heat stress. Microb Ecol 84(4):1224–1235. https://doi.org/10.1007/S00248-021-01929-Y/FIGURES/9 PubMed DOI
Duron O, Morel O, Noël V et al (2018) Tick-bacteria mutualism depends on B vitamin synthesis pathways. Curr Biol 28(12):1896-1902.e5. https://doi.org/10.1016/j.cub.2018.04.038 PubMed DOI
Duron O, Gottlieb Y (2020) Convergence of nutritional symbioses in obligate blood feeders. Trends Parasitol 36(10):816–825. https://doi.org/10.1016/J.PT.2020.07.007 PubMed DOI
Fujisawa S, Murata S, Isezaki M et al (2020) Transcriptome dynamics of blood-fed and starved poultry red mites, Dermanyssus gallinae. Parasitol Int 78:102156. https://doi.org/10.1016/J.PARINT.2020.102156 PubMed DOI
Neuvonen MM, Tamarit D, Näslund K et al (2016) The genome of Rhizobiales bacteria in predatory ants reveals urease gene functions but no genes for nitrogen fixation. Sci Reports 6:39197. https://doi.org/10.1038/srep39197 DOI
Hubert J, Nesvorna M, Sopko B, Smrz J, Klimov P, Erban T (2018) Two populations of mites (Tyrophagus putrescentiae) differ in response to feeding on feces-containing diets. Front Microbiol 9:2590. https://doi.org/10.3389/FMICB.2018.02590/BIBTEX PubMed DOI PMC
Lima-Barbero JF, Díaz-Sanchez S, Sparagano O, Finn RD, de la Fuente J, Villar M (2019) Metaproteomics characterization of the alphaproteobacteria microbiome in different developmental and feeding stages of the poultry red mite Dermanyssus gallinae (De Geer, 1778). Avian Pathol 48(sup1):S52–S59. https://doi.org/10.1080/03079457.2019.1635679 PubMed DOI
Sayed AM, Abdel-Wahab NM, Hassan HM, Abdelmohsen UR (2020) Saccharopolyspora: an underexplored source for bioactive natural products. J Appl Microbiol 128(2):314–329. https://doi.org/10.1111/JAM.14360 PubMed DOI
Parker BJ, Wearsch PA, Veloo ACM, Rodriguez-Palacios A (2020) The genus Alistipes: gut bacteria with emerging implications to inflammation, cancer, and mental health. Front Immunol 11:906. https://doi.org/10.3389/FIMMU.2020.00906 PubMed DOI PMC
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. Microbiol Open 8(6):e00743. https://doi.org/10.1002/MBO3.743 DOI