Bacteria Belonging to Pseudomonas typographi sp. nov. from the Bark Beetle Ips typographus Have Genomic Potential to Aid in the Host Ecology

. 2020 Sep 03 ; 11 (9) : . [epub] 20200903

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid32899185

Grantová podpora
19-09072S Grantová Agentura České Republiky

European Bark Beetle Ips typographus is a secondary pest that affects dead and weakened spruce trees (Picea genus). Under certain environmental conditions, it has massive outbreaks, resulting in the attacks of healthy trees, becoming a forest pest. It has been proposed that the bark beetle's microbiome plays a key role in the insect's ecology, providing nutrients, inhibiting pathogens, and degrading tree defense compounds, among other probable traits yet to be discovered. During a study of bacterial associates from I. typographus, we isolated three strains identified as Pseudomonas from different beetle life stages. A polyphasic taxonomical approach showed that they belong to a new species for which the name Pseudomonas typographi sp nov. is proposed. Genome sequences show their potential to hydrolyze wood compounds and synthesize several vitamins; screening for enzymes production was verified using PNP substrates. Assays in Petri dishes confirmed cellulose and xylan hydrolysis. Moreover, the genomes harbor genes encoding chitinases and gene clusters involved in the synthesis of secondary metabolites with antimicrobial potential. In vitro tests confirmed the capability of the three P. typographi strains to inhibit several Ips beetles' pathogenic fungi. Altogether, these results suggest that P. typographi aids I. typographi nutrition and resistance to fungal pathogens.

Zobrazit více v PubMed

García-Fraile P. Roles of bacteria in the bark beetle holobiont—How do they shape this forest pest? Ann. Appl. Biol. 2018;172 doi: 10.1111/aab.12406. DOI

Six D.L. The Bark Beetle Holobiont: Why Microbes Matter. J. Chem. Ecol. 2013;39:989–1002. doi: 10.1007/s10886-013-0318-8. PubMed DOI

Species Profile Ips Typographus. [(accessed on 3 July 2020)]; Available online: http://www.iucngisd.org/gisd/species.php?sc=1441.

Fabryová A., Kostovčík M., Díez-Méndez A., Jiménez-Gómez A., Celador-Lera L., Saati-Santamaría Z., Sechovcová H., Menéndez E., Kolařik M., García-Fraile P. On the bright side of a forest pest-the metabolic potential of bark beetles’ bacterial associates. Sci. Total Environ. 2018;619–620:9–17. doi: 10.1016/j.scitotenv.2017.11.074. PubMed DOI

Cheng C., Wickham J.D., Chen L., Xu D., Lu M., Sun J. Bacterial microbiota protect an invasive bark beetle from a pine defensive compound. Microbiome. 2018;6 doi: 10.1186/s40168-018-0518-0. PubMed DOI PMC

Boone C.K., Keefover-Ring K., Mapes A.C., Adams A.S., Bohlmann J., Raffa K.F. Bacteria Associated with a Tree-Killing Insect Reduce Concentrations of Plant Defense Compounds. J. Chem. Ecol. 2013;39:1003–1006. doi: 10.1007/s10886-013-0313-0. PubMed DOI

Mattanovich J., Ehrenhofer M., Schafellner C., Tausz M., Fuhrer E. The role of sulphur compounds for breeding success of Ips typographus L. (Col., Scolytidae) on Norway Spruce (Picea abies [L.] Karst.) J. Appl. Entomol. 2001;125:425–431. doi: 10.1046/j.1439-0418.2001.00572.x. DOI

Bozzano L. In: Insect-Fungus Interactions. 1st ed. Wilding N., Collins N.M., Hammond P.M., Webber J.F., editors. Elsevier Ltd.; Amsterdam, The Netherlands: 1988.

Morales-Jiménez J., de León A.V.-P., García-Domínguez A., Martínez-Romero E., Zúñiga G., Hernández-Rodríguez C. Nitrogen-Fixing and Uricolytic Bacteria Associated with the Gut of Dendroctonus rhizophagus and Dendroctonus valens (Curculionidae: Scolytinae) Microb. Ecol. 2013;66:200–210. doi: 10.1007/s00248-013-0206-3. PubMed DOI

Wegensteiner R., Weiser J., Führer E. Observations on the occurrence of pathogens in the bark beetle Ips typographus L. (Col., Scolytidae) J. Appl. Entomol. 1996;120:199–204. doi: 10.1111/j.1439-0418.1996.tb01591.x. DOI

Wegensteiner R., Weiser J. Annual variation of pathogen occurrence and pathogen prevalence in Ips typographus (Coleoptera, Scolytidae) from the BOKU University Forest Demonstration Centre. J. Pest Sci. 2004;77:221–228. doi: 10.1007/s10340-004-0056-3. DOI

Takov D., Pilarska D., Wegensteiner R. Entomopathogens in Ips typographus (Coleoptera: Scolytidae) from Several Spruce Stands in Bulgaria. Acta Zool. Bulg. 2006;58:409–420.

Saati-Santamaría Z., López-Mondéjar R., Jiménez-Gómez A., Díez-Méndez A., Vetrovský T., Igual J.M., Velázquez E., Kolarik M., Rivas R., García-Fraile P. Discovery of phloeophagus beetles as a source of pseudomonas strains that produce potentially new bioactive substances and description of pseudomonas bohemica sp. nov. Front. Microbiol. 2018;9:913. doi: 10.3389/fmicb.2018.00913. PubMed DOI PMC

Kostas B., Thomas A.M. In: Insect Symbiosis. Kostas B., Thomas A.M., editors. Volume 3 CRC Press; Boca Raton, FL, USA: 2003.

Morales-Jiménez J., Zúñiga G., Ramírez-Saad H.C., Hernández-Rodríguez C. Gut-Associated Bacteria Throughout the Life Cycle of the Bark Beetle Dendroctonus rhizophagus Thomas and Bright (Curculionidae: Scolytinae) and Their Cellulolytic Activities. Microb. Ecol. 2012;64:268–278. doi: 10.1007/s00248-011-9999-0. PubMed DOI

Sousa M. On the Multitrophic Interactions between Ips Typographus Their Tree Host, Associated Microorganisms, and a Predatory Medetera Fly. Institutionen för Växtskyddsbiologi, Sveriges Lantbruksuniversitet; Upsala, Sweden: 2019.

Skrodenytee-Arbaciauskiene V., Radziute S., Stunzenas V., Buda V. Erwinia typographi sp. nov., isolated from bark beetle (Ips typographus) gut. Int. J. Syst. Evol. Microbiol. 2012;62:942–948. doi: 10.1099/ijs.0.030304-0. PubMed DOI

Peix A., Ramírez-Bahena M.H., Velázquez E. Historical evolution and current status of the taxonomy of genus Pseudomonas. Infect. Genet. Evol. 2009;9:1132–1147. doi: 10.1016/j.meegid.2009.08.001. PubMed DOI

Marek-Kozaczuk M., Skorupska A. Production of B-group vitamins by plant growth-promoting Pseudomonas fluorescens strain 267 and the importance of vitamins in the colonization and nodulation of red clover. Biol. Fertil. Soils. 2001;33:146–151. doi: 10.1007/s003740000304. DOI

Rivas R., García-Fraile P., Mateos P.F., Martínez-Molina E., Velázquez E. Characterization of xylanolytic bacteria present in the bract phyllosphere of the date palm Phoenix dactylifera. Lett. Appl. Microbiol. 2007;44:181–187. doi: 10.1111/j.1472-765X.2006.02050.x. PubMed DOI

Hall T.A. BioEdit: A user-friendly biological sequence alignment editor and análisis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999;41:95–98.

Kim O.S., Cho Y.J., Lee K., Yoon S.H., Kim M., Na H., Park S.C., Jeon Y.S., Lee J.H., Yi H., et al. Introducing EzTaxon-e: A prokaryotic 16s rRNA gene sequence database with phylotypes that represent uncultured species. Int. J. Syst. Evol. Microbiol. 2012;62:716–721. doi: 10.1099/ijs.0.038075-0. PubMed DOI

Bankevich A., Nurk S., Antipov D., Gurevich A.A., Dvorkin M., Kulikov A.S., Lesin V.M., Nikolenko S.I., Pham S., Prjibelski A.D., et al. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 2012 doi: 10.1089/cmb.2012.0021. PubMed DOI PMC

Kumar S., Stecher G., Li M., Knyaz C., Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol. Biol. Evol. 2018;35:1547–1549. doi: 10.1093/molbev/msy096. PubMed DOI PMC

Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 doi: 10.1093/nar/22.22.4673. PubMed DOI PMC

Larkin M.A., Blackshields G., Brown N.P., Chenna R., Mcgettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., et al. Clustal W and Clustal X version 2.0. Bioinformatics. 2007 doi: 10.1093/bioinformatics/btm404. PubMed DOI

Tamura K., Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 1993;10:512–526. doi: 10.1093/oxfordjournals.molbev.a040023. PubMed DOI

Pritchard L., Glover R.H., Humphris S., Elphinstone J.G., Toth I.K. Genomics and taxonomy in diagnostics for food security: Soft-rotting enterobacterial plant pathogens. Anal. Methods. 2015;8:12–24. doi: 10.1039/C5AY02550H. DOI

Warnes G.R., Bolker B., Bonebakker L., Gentleman R., Huber W., Liaw A., Lumley T., Maechler M., Magnusson A., Moeller S., et al. gplots: Various R Programming Tools for Plotting Data. R Package Version 3.0.4. [(accessed on 2 September 2020)]; Available online: https://CRAN.R-project.org/package=gplots.

Meier-Kolthoff J.P., Auch A.F., Klenk H.-P., Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform. 2013;14:60. doi: 10.1186/1471-2105-14-60. PubMed DOI PMC

Aziz R.K., Bartels D., Best A.A., DeJongh M., Disz T., Edwards R.A., Formsma K., Gerdes S., Glass E.M., Kubal M., et al. The RAST Server: Rapid Annotations using Subsystems Technology. BMC Genom. 2008;9:75. doi: 10.1186/1471-2164-9-75. PubMed DOI PMC

Aramaki T., Blanc-Mathieu R., Endo H., Ohkubo K., Kanehisa M., Goto S., Ogata H. KofamKOALA: KEGG Ortholog assignment based on profile HMM and adaptive score threshold. Bioinformatics. 2020;36:2251–2252. doi: 10.1093/bioinformatics/btz859. PubMed DOI PMC

Overbeek R., Olson R., Pusch G.D., Olsen G.J., Davis J.J., Disz T., Edwards R.A., Gerdes S., Parrello B., Shukla M., et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST) Nucleic Acids Res. 2014;42:D206–D214. doi: 10.1093/nar/gkt1226. PubMed DOI PMC

Blin K., Shaw S., Steinke K., Villebro R., Ziemert N., Lee S.Y., Medema M.H., Weber T. antiSMASH 5.0: Updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res. 2019;47:W81–W87. doi: 10.1093/nar/gkz310. PubMed DOI PMC

Zhang H., Yohe T., Huang L., Entwistle S., Wu P., Yang Z., Busk P.K., Xu Y., Yin Y. dbCAN2: A meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 2018;46:W95–W101. doi: 10.1093/nar/gky418. PubMed DOI PMC

Le Normand M., Edlund U., Holmbom B., Ek M. Hot-water extraction and characterization of spruce bark non-cellulosic polysaccharides. Nord. Pulp Pap. Res. J. 2012;27:18–23. doi: 10.3183/npprj-2012-27-01-p018-023. DOI

BioFuel Region: Basic Chemical composition of the biomass components of pine, spruce and birch. [(accessed on 2 September 2020)]; Available online: http://biofuelregion.se/wp-content/uploads/2017/01/1_2_IS_2013-01-31_Basic_chemical_composition.pdf.

Mateos P.F., Jimenez-Zurdo J.I., Chen J., Squartini A.S., Haack S.K., Martinez-Molina E., Hubbell D.H., Dazzo F.B. Cell-associated pectinolytic and cellulolytic enzymes in Rhizobium leguminosarum biovar trifolii. Appl. Environ. Microbiol. 1992;58:1816–1822. doi: 10.1128/AEM.58.6.1816-1822.1992. PubMed DOI PMC

García-Fraile P., Rivas R., Willems A., Peix A., Martens M., Martínez-Molina E., Mateos P.F., Velázquez E. Rhizobium cellulosilyticum sp. nov., isolated from sawdust of Populus alba. Int. J. Syst. Evol. Microbiol. 2007 doi: 10.1099/ijs.0.64680-0. PubMed DOI

Kubátová A., Dvořák L. Entomopathogenic fungi associated with insect hibernating in underground shelters The distribution of scorpion flies of the genus Panorpa in the West Palaearctic View project Libor Dvořák Municipal Museum Mariánské Lázně, Czech Republic. Czech Mycol. 2005;57:221–237. doi: 10.33585/cmy.57303. DOI

Pažoutová S., Šrůtka P., Holuša J., Chudíčková M., Kolařík M. Diversity of xylariaceous symbionts in Xiphydria woodwasps: Role of vector and a host tree. Fungal Ecol. 2010;3:392–401. doi: 10.1016/j.funeco.2010.07.002. DOI

Wegensteiner R., Wermelinger B., Herrmann M. Bark Beetles: Biology and Ecology of Native and Invasive Species. Elsevier Inc.; Amsterdam, The Netherlands: 2015. Natural enemies of bark beetles: Predators, parasitoids, pathogens, and nematodes; pp. 247–304.

Jiménez-Gómez A., Saati-Santamaría Z., Igual J.M., Rivas R., Mateos P.F., García-Fraile P. Genome insights into the novel species Microvirga brassicacearum, a rapeseed endophyte with biotechnological potential. Microorganisms. 2019;7:354. doi: 10.3390/microorganisms7090354. PubMed DOI PMC

Doetsch R.N. Determinative methods of light microscopy. In: Gerdhardt P., Murray R.G.E., Costilow R.N., Nester E.W., Wood W.A., Krieg N.R., Phillips G.B., editors. Manual of Methods for General Bacteriology. American Society for Microbiology; Washington, DC, USA: 1981. pp. 21–33.

García-Fraile P., Chudíčková M., Benada O., Pikula J., Kolařík M. Serratia myotis sp. nov. and Serratia vespertilionis sp. nov., isolated from bats hibernating in caves. Int. J. Syst. Evol. Microbiol. 2015;65:90–94. doi: 10.1099/ijs.0.066407-0. PubMed DOI

Kovacs N. Identification of Pseudomonas pyocyanea by the Oxidase Reaction. Nature. 1956;178:703. doi: 10.1038/178703a0. PubMed DOI

Ramírez-Bahena M.-H., Cuesta M.J., Flores-Félix J.D., Mulas R., Rivas R., Castro-Pinto J., Brañas J., Mulas D., González-Andrés F., Velázquez E., et al. Pseudomonas helmanticensis sp. nov., isolated from forest soil. Int. J. Syst. Evol. Microbiol. 2014;64:2338–2345. doi: 10.1099/ijs.0.063560-0. PubMed DOI

Ait Tayeb L., Ageron E., Grimont F., Grimont P.A.D. Molecular phylogeny of the genus Pseudomonas based on rpoB sequences and application for the identification of isolates. Microbiol. Res. 2005;156:763–773. doi: 10.1016/j.resmic.2005.02.009. PubMed DOI

Mulet M., Bennasar A., Lalucat J., García-Valdés E. An rpoD-based PCR procedure for the identification of Pseudomonas species and for their detection in environmental samples. Mol. Cell. Probes. 2009;23:140–147. doi: 10.1016/j.mcp.2009.02.001. PubMed DOI

Mulet M., Lalucat J., García-Valdés E. DNA sequence-based analysis of the Pseudomonas species. Environ. Microbiol. 2010;12:1513–1530. doi: 10.1111/j.1462-2920.2010.02181.x. PubMed DOI

Mulet M., Gomila M., Lemaitre B., Lalucat J., García-Valdés E. Taxonomic characterisation of Pseudomonas strain L48 and formal proposal of Pseudomonas entomophila sp. nov. Syst. Appl. Microbiol. 2012;35:145–149. doi: 10.1016/j.syapm.2011.12.003. PubMed DOI

Ramos E., Ramírez-Bahena M.-H., Valverde A., Velázquez E., Zúñiga D., Velezmoro C., Peix A. Pseudomonas punonensis sp. nov., isolated from straw. Int. J. Syst. Evol. Microbiol. 2013;63:1834–1839. doi: 10.1099/ijs.0.042119-0. PubMed DOI

Toro M., Ramírez-Bahena M.-H., Cuesta M.J., Velázquez E., Peix A. Pseudomonas guariconensis sp. nov., isolated from rhizospheric soil. Int. J. Syst. Evol. Microbiol. 2013;63:4413–4420. doi: 10.1099/ijs.0.051193-0. PubMed DOI

Menéndez E., Ramírez-Bahena M.H., Fabryová A., Igual J.M., Benada O., Mateos P.F., Peix A., Kolařík M., García-Fraile P. Pseudomonas coleopterorum sp. nov., a cellulase-producing bacterium isolated from the bark beetle Hylesinus fraxini. Int. J. Syst. Evol. Microbiol. 2015;65:2852–2858. doi: 10.1099/ijs.0.000344. PubMed DOI

Peix A. Pseudomonas rhizosphaerae sp. nov., a novel species that actively solubilizes phosphate in vitro. Int. J. Syst. Evol. Microbiol. 2003;53:2067–2072. doi: 10.1099/ijs.0.02703-0. PubMed DOI

Mulet M., Sánchez D., Lalucat J., Lee K., García-Valdés E. Pseudomonas alkylphenolica sp. nov., a bacterial species able to form special aerial structures when grown on p-cresol. Int. J. Syst. Evol. Microbiol. 2015;65:4013–4018. doi: 10.1099/ijsem.0.000529. PubMed DOI

Behrendt U., Ulrich A., Schumann P. Fluorescent pseudomonads associated with the phyllosphere of grasses; Pseudomonas trivialis sp. nov., Pseudomonas poae sp. nov. and Pseudomonas congelans sp. nov. Int. J. Syst. Evol. Microbiol. 2003;53:1461–1469. doi: 10.1099/ijs.0.02567-0. PubMed DOI

Richter M., Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc. Natl. Acad. Sci. USA. 2009;106:19126–19131. doi: 10.1073/pnas.0906412106. PubMed DOI PMC

Chun J., Oren A., Ventosa A., Christensen H., Arahal D.R., da Costa M.S., Rooney A.P., Yi H., Xu X.W., De Meyer S., et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int. J. Syst. Evol. Microbiol. 2018;68:461–466. doi: 10.1099/ijsem.0.002516. PubMed DOI

Menendez E., Garcia-Fraile P., Rivas R. Biotechnological applications of bacterial cellulases. AIMS Bioeng. 2015;2:163–182. doi: 10.3934/bioeng.2015.3.163. DOI

Collins T., Gerday C., Feller G. Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiol. Rev. 2005;29:3–23. doi: 10.1016/j.femsre.2004.06.005. PubMed DOI

Zhou M., Guo P., Wang T., Gao L., Yin H., Cai C., Gu J., Lü X. Metagenomic mining pectinolytic microbes and enzymes from an apple pomace-adapted compost microbial community. Biotechnol. Biofuels. 2017;10:1–15. doi: 10.1186/s13068-017-0885-y. PubMed DOI PMC

Bertoldo C., Antranikian G. Starch-hydrolyzing enzymes from thermophilic archaea and bacteria. Curr. Opin. Chem. Biol. 2002;6:151–160. doi: 10.1016/S1367-5931(02)00311-3. PubMed DOI

Boller T. Antimicrobial functions of the plant hydrolases, chitinase and ß-1,3-glucanase. Developments in Plant Pathology. In: Fritig B., Legrand M., editors. Mechanisms of Plant Defense Responses. Springer; Dordrecht, The Netherlands: 1993. pp. 391–400.

Arora N.K., Khare E., Oh J.H., Kang S.C., Maheshwari D.K. Diverse mechanisms adopted by fluorescent Pseudomonas PGC2 during the inhibition of Rhizoctonia solani and Phytophthora capsici. World J. Microbiol. Biotechnol. 2008;24:581–585. doi: 10.1007/s11274-007-9505-5. DOI

Rojas Murcia N., Lee X., Waridel P., Maspoli A., Imker H.J., Chai T., Walsh C.T., Reimmann C. The Pseudomonas aeruginosa antimetabolite L -2-amino-4-methoxy-trans-3-butenoic acid (AMB) is made from glutamate and two alanine residues via a thiotemplate-linked tripeptide precursor. Front. Microbiol. 2015;6:170. doi: 10.3389/fmicb.2015.00170. PubMed DOI PMC

Baars O., Zhang X., Gibson M.I., Stone A.T., Morel F.M.M., Seyedsayamdost M.R. Crochelins: Siderophores with an Unprecedented Iron-Chelating Moiety from the Nitrogen-Fixing Bacterium Azotobacter chroococcum. Angew. Chem. Int. Ed. Engl. 2018;57:536–541. doi: 10.1002/anie.201709720. PubMed DOI

Lee X., Reimmann C., Greub G., Sufrin J., Croxatto A. The Pseudomonas aeruginosa toxin L-2-amino-4-methoxy-trans-3-butenoic acid inhibits growth and induces encystment in Acanthamoeba castellanii. Microbes Infect. 2012;14:268–272. doi: 10.1016/j.micinf.2011.10.004. PubMed DOI

Sulochana M.B., Jayachandra S.Y., Kumar S.K.A., Dayanand A. Antifungal attributes of siderophore produced by the Pseudomonas aeruginosa JAS-25. J. Basic Microbiol. 2013;54:418–424. doi: 10.1002/jobm.201200770. PubMed DOI

Cvikrová M., Malá J., Hrubcová M., Eder J. Soluble and cell wall-bound phenolics and lignin in Ascocalyx abietina infected Norway spruces. Plant Sci. 2006;170:563–570. doi: 10.1016/j.plantsci.2005.10.011. DOI

Adams A.S., Aylward F.O., Adams S.M., Erbilgin N., Aukema B.H., Currie C.R., Suen G., Raffa K.F. Mountain pine beetles colonizing historical and naïve host trees are associated with a bacterial community highly enriched in genes contributing to terpene metabolism. Appl. Environ. Microbiol. 2013;79:3468–3475. doi: 10.1128/AEM.00068-13. PubMed DOI PMC

Sagot B., Gaysinski M., Mehiri M., Guigonis J.-M., Le Rudulier D., Alloing G. Osmotically induced synthesis of the dipeptide N-acetylglutaminylglutamine amide is mediated by a new pathway conserved among bacteria. Proc. Natl. Acad. Sci. USA. 2010;107:12652–12657. doi: 10.1073/pnas.1003063107. PubMed DOI PMC

Sedkova N., Tao L., Rouvière P.E., Cheng Q. Diversity of Carotenoid Synthesis Gene Clusters from Environmental Enterobacteriaceae Strains. Appl. Environ. Microbiol. 2005;71:8141–8146. doi: 10.1128/AEM.71.12.8141-8146.2005. PubMed DOI PMC

Sloan D.B., Moran N.A. Endosymbiotic bacteria as a source of carotenoids in whiteflies. Biol. Lett. 2012;8:986–989. doi: 10.1098/rsbl.2012.0664. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...