A novel Bartonella-like bacterium forms an interdependent mutualistic symbiosis with its host, the stored-product mite Tyrophagus putrescentiae

. 2024 Mar 19 ; 9 (3) : e0082923. [epub] 20240221

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38380907

Grantová podpora
GA19-09998 Grantová Agentura České Republiky (GAČR)
MZE-RO0423 Ministerstvo Zemědělství (Ministry of Agriculture)

A novel Bartonella-like symbiont (BLS) of Tyrophagus putrescentiae was characterized. BLS formed a separate cluster from the Bartonella clade together with an ant symbiont. BLS was present in mite bodies (103 16S DNA copies/mite) and feces but was absent in eggs. This indicated the presence of the BLS in mite guts. The BLS showed a reduction in genome size (1.6 Mb) and indicates gene loss compared to Bartonella apis. The BLS can be interacted with its host by using host metabolic pathways (e.g., the histidine and arginine metabolic pathways) as well as by providing its own metabolic pathways (pantothenate and lipoic acid) to the host, suggesting the existence of a mutualistic association. Our experimental data further confirmed these potential mutualistic nutritional associations, as cultures of T. putrescentiae with low BLS abundance showed the strongest response after the addition of vitamins. Despite developing an arguably tight dependency on its host, the BLS has probably retained flagellar mobility, as evidenced by the 32 proteins enriched in KEGG pathways associated with flagellar assembly or chemotaxis (e.g., fliC, flgE, and flgK, as highly expressed genes). Some of these proteins probably also facilitate adhesion to host gut cells. The microcin C transporter was identified in the BLS, suggesting that microcin C may be used in competition with other gut bacteria. The 16S DNA sequence comparison indicated a mite clade of BLSs with a broad host range, including house dust and stored-product mites. Our phylogenomic analyses identified a unique lineage of arachnid specific BLSs in mites and scorpions.IMPORTANCEA Bartonella-like symbiont was found in an astigmatid mite of allergenic importance. We assembled the genome of the bacterium from metagenomes of different stored-product mite (T. putrescentiae) cultures. The bacterium provides pantothenate and lipoic acid to the mite host. The vitamin supply explains the changes in the relative abundance of BLSs in T. putrescentiae as the microbiome response to nutritional or pesticide stress, as observed previously. The phylogenomic analyses of available 16S DNA sequences originating from mite, scorpion, and insect samples identified a unique lineage of arachnid specific forming large Bartonella clade. BLSs associated with mites and a scorpion. The Bartonella clade included the previously described Ca. Tokpelaia symbionts of ants.

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Okaro U, Addisu A, Casanas B, Anderson B. 2017. Bartonella species, an emerging cause of blood-culture-negative endocarditis. Clin Microbiol Rev 30:709–746. doi:10.1128/CMR.00013-17 PubMed DOI PMC

Segers FHID, Kesnerova L, Kosoy M, Engel P. 2017. Genomic changes associated with the evolutionary transition of an insect gut symbiont into a blood-borne pathogen. ISME J 11:1232–1244. doi:10.1038/ismej.2016.201 PubMed DOI PMC

Kesnerova L, Moritz R, Engel P. 2016. Bartonella apis sp. nov., a honey bee gut symbiont of the class Alphaproteobacteria. Int J Syst Evol Microbiol 66:414–421. doi:10.1099/ijsem.0.000736 PubMed DOI

Liu Y, Chen J, Lang H, Zheng H. 2022. Bartonella choladocola sp. nov. and Bartonella apihabitans sp. nov., two novel species isolated from honey bee gut. Syst Appl Microbiol 45:126372. doi:10.1016/j.syapm.2022.126372 PubMed DOI

Russell JA, Moreau CS, Goldman-Huertas B, Fujiwara M, Lohman DJ, Pierce NE. 2009. Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc Natl Acad Sci U S A 106:21236–21241. doi:10.1073/pnas.0907926106 PubMed DOI PMC

Zhukova M, Sapountzis P, Schiott M, Boomsma JJ. 2022. Phylogenomic analysis and metabolic role reconstruction of mutualistic Rhizobiales hindgut symbionts of Acromyrmex leaf-cutting ants. FEMS Microbiol Ecol 98:fiac084. doi:10.1093/femsec/fiac084 PubMed DOI

Stoll S, Gadau J, Gross R, Feldhaar H. 2007. Bacterial microbiota associated with ants of the genus Tetraponera. Biol J Linn Soc 90:399–412. doi:10.1111/j.1095-8312.2006.00730.x DOI

Larson HK, Goffredi SK, Parra EL, Vargas O, Pinto-Tomas AA, McGlynn TP. 2014. Distribution and dietary regulation of an associated facultative Rhizobiales-related bacterium in the omnivorous giant tropical ant, Paraponera clavata. Naturwissenschaften 101:397–406. doi:10.1007/s00114-014-1168-0 PubMed DOI

Neuvonen M-M, Tamarit D, Näslund K, Liebig J, Feldhaar H, Moran NA, Guy L, Andersson SGE. 2016. The genome of Rhizobiales bacteria in predatory ants reveals urease gene functions but no genes for nitrogen fixation. Sci Rep 6:39197. doi:10.1038/srep39197 PubMed DOI PMC

Lukasik P, Newton JA, Sanders JG, Hu Y, Moreau CS, Kronauer DJC, O’Donnell S, Koga R, Russell JA. 2017. The structured diversity of specialized gut symbionts of the new world army ants. Mol Ecol 26:3808–3825. doi:10.1111/mec.14140 PubMed DOI

Bisch G, Neuvonen M-M, Pierce NE, Russell JA, Koga R, Sanders JG, Lukasik P, Andersson SGE. 2018. Genome evolution of Bartonellaceae symbionts of ants at the opposite ends of the trophic scale. Genome Biol Evol 10:1687–1704. doi:10.1093/gbe/evy126 PubMed DOI PMC

Kopecky J, Nesvorna M, Hubert J. 2014. Bartonella-like bacteria carried by domestic mite species. Exp Appl Acarol 64:21–32. doi:10.1007/s10493-014-9811-1 PubMed DOI

Hubert Jan, 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

Hubert J, Nesvorna M, Kopecky J, Sagova-Mareckova M, Poltronieri P. 2015. Carpoglyphus lactis (Acari: Astigmata) from various dried fruits differed in associated micro-organisms. J Appl Microbiol 118:470–484. doi:10.1111/jam.12714 PubMed DOI

Valerio CR, Murray P, Arlian LG, Slater JE. 2005. Bacterial 16S ribosomal DNA in house dust mite cultures. J Allergy Clin Immunol 116:1296–1300. doi:10.1016/j.jaci.2005.09.046 PubMed DOI

Hubert J, Erban T, Kopecky J, Sopko B, Nesvorna M, Lichovnikova M, Schicht S, Strube C, Sparagano O. 2017. Comparison of microbiomes between red poultry mite populations (Dermanyssus gallinae): predominance of Bartonella-like bacteria. Microb Ecol 74:947–960. doi:10.1007/s00248-017-0993-z PubMed DOI

Hubert J, Erban T, Kamler M, Kopecky J, Nesvorna M, Hejdankova S, Titera D, Tyl J, Zurek L. 2015. Bacteria detected in the honeybee parasitic mite Varroa destructor collected from beehive winter debris. J Appl Microbiol 119:640–654. doi:10.1111/jam.12899 PubMed DOI

Colloff MJ. 2009. Dust mites. CSIRO Publishing, Collingwood, VIC.

Hughes AM. 1976. The mites of stored food and houses. 2nd edn. Technical Bulletin 9 of the Ministry of Agriculture, Fisheries and Food. Her Majesty’s Stationery Office, London.

Hubert J, Nesvorna M, Green SJ, Klimov PB. 2021. Microbial communities of stored product mites: variation by species and population. Microb Ecol 81:506–522. doi:10.1007/s00248-020-01581-y PubMed DOI

Vrtala S. 2022. Allergens from house dust and storage mites. Allergo J Int 31:267–271. doi:10.1007/s40629-022-00226-5 DOI

Hubert J, Nesvorna M, Klimov P, Dowd SE, Sopko B, Erban T. 2019. Differential allergen expression in three Tyrophagus putrescentiae strains inhabited by distinct microbiome. Allergy 74:2502–2507. doi:10.1111/all.13921 PubMed DOI

Lee J, Kim JY, Yi M-H, Hwang Y, Lee I-Y, Nam S-H, Yong D, Yong T-S. 2019. Comparative microbiome analysis of Dermatophagoides farinae, Dermatophagoides pteronyssinus, and Tyrophagus putrescentiae. J Allergy Clin Immunol 143:1620–1623. doi:10.1016/j.jaci.2018.10.062 PubMed DOI

Yi M, Kim M, Yong T-S, Kim JY. 2023. Investigating the microbiome of house dust mites in South Korea. Front Allergy 4:1240727. doi:10.3389/falgy.2023.1240727 PubMed DOI PMC

Erban T, Ledvinka O, Nesvorna M, Hubert J. 2017. Experimental manipulation shows a greater influence of population than dietary perturbation on the microbiome of Tyrophagus putrescentiae. Appl Environ Microbiol 83:e00128-17. doi:10.1128/AEM.00128-17 PubMed DOI PMC

Hubert J, Nesvorna M, Bostlova M, Sopko B, Green SJ, Phillips TW. 2023. The effect of residual pesticide application on microbiomes of the storage mite Tyrophagus putrescentiae. Microb Ecol 85:1527–1540. doi:10.1007/s00248-022-02072-y PubMed DOI

Nesvorna M, Bittner V, Hubert J. 2019. The mite Tyrophagus putrescentiae hosts population-specific microbiomes that respond weakly to starvation. Microb Ecol 77:488–501. doi:10.1007/s00248-018-1224-y PubMed DOI

Hubert J, Nesvorna M, Sopko B, Green SJ. 2023. Diet modulation of the microbiome of the pest storage mite Tyrophagus putrescentiae. FEMS Microbiol Ecol 99:fiad011. doi:10.1093/femsec/fiad011 PubMed DOI

Paris L, Peghaire E, Mone A, Diogon M, Debroas D, Delbac F, El Alaoui H. 2020. Honeybee gut microbiota dysbiosis in pesticide/parasite co-exposures is mainly induced by Nosema ceranae. J Invertebr Pathol 172:107348. doi:10.1016/j.jip.2020.107348 PubMed DOI

Hubert J, Bicianova M, Ledvinka O, Kamler M, Lester PJ, Nesvorna M, Kopecky J, Erban T. 2017. Changes in the bacteriome of honey bees associated with the parasite Varroa destructor, and pathogens Nosema and Lotmaria passim. Microb Ecol 73:685–698. doi:10.1007/s00248-016-0869-7 PubMed DOI

Manni M, Berkeley MR, Seppey M, Zdobnov EM. 2021. BUSCO: assessing genomic data quality and beyond. Curr Protoc 1:e323. doi:10.1002/cpz1.323 PubMed DOI

Dehio C. 2008. Infection-associated type IV secretion systems of Bartonella and their diverse roles in host cell interaction. Cell Microbiol 10:1591–1598. doi:10.1111/j.1462-5822.2008.01171.x PubMed DOI PMC

Vayssier-Taussat M, Le Rhun D, Deng HK, Biville F, Cescau S, Danchin A, Marignac G, Lenaour E, Boulouis HJ, Mavris M, Arnaud L, Yang H, Wang J, Quebatte M, Engel P, Saenz H, Dehio C. 2010. The Trw type IV secretion system of Bartonella mediates host-specific adhesion to erythrocytes. PLoS Pathog 6:e1000946. doi:10.1371/journal.ppat.1000946 PubMed DOI PMC

Quebatte M, Dehio C. 2019. Bartonella gene transfer agent: evolution, function, and proposed role in host adaptation. Cell Microbiol 21:e13068. doi:10.1111/cmi.13068 PubMed DOI PMC

Tamarit D, Neuvonen M-M, Engel P, Guy L, Andersson SGE. 2018. Origin and evolution of the Bartonella gene transfer agent. Mol Biol Evol 35:451–464. doi:10.1093/molbev/msx299 PubMed DOI

Quebatte M, Christen M, Harms A, Korner J, Christen B, Dehio C. 2017. Gene transfer agent promotes evolvability within the fittest subpopulation of a bacterial pathogen. Cell Syst 4:611–621. doi:10.1016/j.cels.2017.05.011 PubMed DOI PMC

Green SJ, Nesvorna M, Hubert J. 2022. The negative effects of feces-associated microorganisms on the fitness of the stored product mite Tyrophagus putrescentiae. Front Microbiol 13:756286. doi:10.3389/fmicb.2022.756286 PubMed DOI PMC

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. doi:10.3389/fmicb.2018.02590 PubMed DOI PMC

Klimov P, Molva V, Nesvorna M, Pekar S, Shcherbachenko E, Erban T, Hubert J. 2019. Dynamics of the microbial community during growth of the house dust mite Dermatophagoides farinae in culture. FEMS Microbiol Ecol 95:11. doi:10.1093/femsec/fiz153 PubMed DOI

Hubert J, Nesvorna M, Kopecky J, Erban T, Klimov P. 2019. Population and culture age influence the microbiome profiles of house dust mites. Microb Ecol 77:1048–1066. doi:10.1007/s00248-018-1294-x PubMed DOI

Sudakaran S, Kost C, Kaltenpoth M. 2017. Symbiont acquisition and replacement as a source of ecological innovation. Trends Microbiol 25:375–390. doi:10.1016/j.tim.2017.02.014 PubMed DOI

Martinson VG, Moy J, Moran NA. 2012. Establishment of characteristic gut bacteria during development of the honeybee worker. Appl Environ Microbiol 78:2830–2840. doi:10.1128/AEM.07810-11 PubMed DOI PMC

Sapountzis P, Zhukova M, Hansen LH, Sorensen SJ, Schiott M, Boomsma JJ. 2015. Acromyrmex leaf-cutting ants have simple gut microbiota with nitrogen-fixing potential. Appl Environ Microbiol 81:5527–5537. doi:10.1128/AEM.00961-15 PubMed DOI PMC

Sobotnik J, Alberti G, Weyda F, Hubert J. 2008. Ultrastructure of the digestive tract in Acarus siro (Acari: Acaridida). J Morphol 269:54–71. doi:10.1002/jmor.10573 PubMed DOI

Raymann K, Moran NA. 2018. The role of the gut microbiome in health and disease of adult honey bee workers. Curr Opin Insect Sci 26:97–104. doi:10.1016/j.cois.2018.02.012 PubMed DOI PMC

Tang Q, Li W, Wang Z, Dong Z, Li X, Li J, Huang Q, Cao Z, Gong W, Zhao Y, Wang M, Guo J. 2023. Gut microbiome helps honeybee (Apis mellifera) resist the stress of toxic nectar plant (Bidens pilosa) exposure: evidence for survival and immunity. Environ Microbiol 25:2020–2031. doi:10.1111/1462-2920.16436 PubMed DOI

Castelli L, Branchiccela B, Garrido M, Invernizzi C, Porrini M, Romero H, Santos E, Zunino P, Antunez K. 2020. Impact of nutritional stress on honeybee gut microbiota, immunity, and Nosema ceranae infection. Microb Ecol 80:908–919. doi:10.1007/s00248-020-01538-1 PubMed DOI

Bantysh O, Serebryakova M, Makarova KS, Dubiley S, Datsenko KA, Severinov K. 2014. Enzymatic synthesis of bioinformatically predicted microcin C-like compounds encoded by diverse bacteria. mBio 5:e01059-14. doi:10.1128/mBio.01059-14 PubMed DOI PMC

Severinov K, Nair SK. 2012. Microcin C: biosynthesis and mechanisms of bacterial resistance. Future Microbiol 7:281–289. doi:10.2217/fmb.11.148 PubMed DOI PMC

Severinov K, Semenova E, Kazakov A, Kazakov T, Gelfand MS. 2007. Low-molecular-weight post-translationally modified microcins. Mol Microbiol 65:1380–1394. doi:10.1111/j.1365-2958.2007.05874.x PubMed DOI

Xiong Q, Wan A-Y, Liu X, Fung C-H, Xiao X, Malainual N, Hou J, Wang L, Wang M, Yang KY, Cui Y, Leung E-H, Nong W, Shin S-K, Au S-N, Jeong KY, Chew F-T, Hui J-L, Leung T-F, Tungtrongchitr A, Zhong N, Liu Z, Tsui S-W. 2022. Comparative genomics reveals insights into the divergent evolution of astigmatic mites and household pest adaptations. Mol Biol Evol 39:msac097. doi:10.1093/molbev/msac097 PubMed DOI PMC

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

Erban T, Hubert J. 2015. Two-dimensional gel proteomic analysis of Dermatophagoides farinae feces. Exp Appl Acarol 65:73–87. doi:10.1007/s10493-014-9848-1 PubMed DOI

Hubert J, Nesvorna M, Pekar S, Green SJ, Klimov PB. 2021. Cardinium inhibits Wolbachia in its mite host, Tyrophagus putrescentiae, and affects host fitness. FEMS Microbiol Ecol 97:10. doi:10.1093/femsec/fiab123 PubMed DOI

Hubert J, Vrtala S, Sopko B, Dowd SE, He Q, Klimov PB, Harant K, Talacko P, Erban T. 2023. Predicting Blomia tropicalis allergens using a multiomics approach. Clin Transl Allergy 13:e12302. doi:10.1002/clt2.12302 PubMed DOI PMC

Krueger F. 2021. Trim Galore. Babraham Bioinformatics. https://www.bioinformatics.babraham.ac.uk/projects/trim_galore/.

Andrews S. 2019. FastQC: a quality control tool for high throughput sequence data. Babraham Bioinformatics. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.

Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25. doi:10.1186/gb-2009-10-3-r25 PubMed DOI PMC

Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. doi:10.1038/nmeth.1923 PubMed DOI PMC

Li H. 2018. Minimap2: pairwise alignment for nucleotide sequences, version 5. arXiv. doi:10.48550/arXiv.1708.01492 PubMed DOI PMC

Boetzer M, Pirovano W. 2014. SSPACE-LongRead: scaffolding bacterial draft genomes using long read sequence information. BMC Bioinformatics 15:211. doi:10.1186/1471-2105-15-211 PubMed DOI PMC

Xu M, Guo L, Gu S, Wang O, Zhang R, Peters BA, Fan G, Liu X, Xu X, Deng L, Zhang Y. 2020. TGS-GapCloser: a fast and accurate gap closer for large genomes with low coverage of error-prone long reads. Gigascience 9:giaa094. doi:10.1093/gigascience/giaa094 PubMed DOI PMC

Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJM, Birol I. 2009. ABySS: a parallel assembler for short read sequence data. Genome Res 19:1117–1123. doi:10.1101/gr.089532.108 PubMed DOI PMC

Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, Cuomo CA, Zeng Q, Wortman J, Young SK, Earl AM. 2014. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9:e112963. doi:10.1371/journal.pone.0112963 PubMed DOI PMC

Seemann T. 2014. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069. doi:10.1093/bioinformatics/btu153 PubMed DOI

Tanizawa Y, Fujisawa T, Nakamura Y. 2018. DFAST: a flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics 34:1037–1039. doi:10.1093/bioinformatics/btx713 PubMed DOI PMC

Kanehisa M, Sato Y, Morishima K. 2016. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 428:726–731. doi:10.1016/j.jmb.2015.11.006 PubMed DOI

Kanehisa M, Goto S. 2000. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30. doi:10.1093/nar/28.1.27 PubMed DOI PMC

Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walter MC, Rattei T, Mende DR, Sunagawa S, Kuhn M, Jensen LJ, von Mering C, Bork P. 2016. eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res 44:D286–D293. doi:10.1093/nar/gkv1248 PubMed DOI PMC

Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH, Koren S, Phillippy AM. 2016. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol 17:132. doi:10.1186/s13059-016-0997-x PubMed DOI PMC

Olm MR, Brown CT, Brooks B, Banfield JF. 2017. dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J 11:2864–2868. doi:10.1038/ismej.2017.126 PubMed DOI PMC

Eddy SR. 2011. Accelerated profile HMM searches. PLoS Comput Biol 7:e1002195. doi:10.1371/journal.pcbi.1002195 PubMed DOI PMC

Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. 2009. BLAST+: architecture and applications. BMC Bioinformatics 10:421. doi:10.1186/1471-2105-10-421 PubMed DOI PMC

Edgar RC. 2022. Muscle5: high-accuracy alignment ensembles enable unbiased assessments of sequence homology and phylogeny. Nat Commun 13:6968. doi:10.1038/s41467-022-34630-w PubMed DOI PMC

Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. doi:10.1093/sysbio/syq010 PubMed DOI

Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW, Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119. doi:10.1186/1471-2105-11-119 PubMed DOI PMC

Steinegger M, Söding J. 2017. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat Biotechnol 35:1026–1028. doi:10.1038/nbt.3988 PubMed DOI

Kreft L, Botzki A, Coppens F, Vandepoele K, Van Bel M. 2017. PhyD3: a phylogenetic tree viewer with extended phyloXML support for functional genomics data visualization. Bioinformatics 33:2946–2947. doi:10.1093/bioinformatics/btx324 PubMed DOI

Finn RD, Clements J, Eddy SR. 2011. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–W37. doi:10.1093/nar/gkr367 PubMed DOI PMC

Notredame C, Higgins DG, Heringa J. 2000. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217. doi:10.1006/jmbi.2000.4042 PubMed DOI

Kopecky J, Nesvorna M, Mareckova-Sagova M, Hubert J. 2014. The effect of antibiotics on associated bacterial community of stored product mites. PLoS ONE 9:e112919. doi:10.1371/journal.pone.0112919 PubMed DOI PMC

Hubert J, Doleckova-Maresova L, Hyblová J, Kudlikova I, Stejskal V, Mares M. 2005. In vitro and in vivo inhibition of α-amylases of stored-product mite Acarus siro. Exp Appl Acarol 35:281–291. doi:10.1007/s10493-004-7834-8 PubMed DOI

Oksanen J. 2022. vegan: an R package for community ecologists. GitHub. https://github.com/vegandevs/vegan.

Hammer O. 2020. Past 4 - the past of the future. Natural History Museum, University of Oslo, Oslo. https://www.nhm.uio.no/english/research/resources/past/.

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