Antimicrobial resistance is a worldwide problem that threatens the effectiveness of treatments for microbial infection. Consequently, it is essential to study unexplored niches that can serve for the isolation of new microbial strains able to produce antimicrobial compounds to develop new drugs. Bark beetles live in phloem of host trees and establish symbioses with microorganisms that provide them with nutrients. In addition, some of their associated bacteria play a role in the beetle protection by producing substances that inhibit antagonists. In this study the capacity of several bacterial strains, isolated from the bark beetles Ips acuminatus, Pityophthorus pityographus Cryphalus piceae, and Pityogenes bidentatus, to produce antimicrobial compounds was analyzed. Several isolates exhibited the capacity to inhibit Gram-positive and Gram-negative bacteria, as well as fungi. The genome sequence analysis of three Pseudomonas isolates predicted the presence of several gene clusters implicated in the production of already described antimicrobials and moreover, the low similarity of some of these clusters with those previously described, suggests that they encode new undescribed substances, which may be useful for developing new antimicrobial agents. Moreover, these bacteria appear to have genetic machinery for producing antitumoral and antiviral substances. Finally, the strain IA19T showed to represent a new species of the genus Pseudomonas. The 16S rRNA gene sequence analysis showed that its most closely related species include Pseudomonas lutea, Pseudomonas graminis, Pseudomonas abietaniphila and Pseudomonas alkylphenolica, with 98.6, 98.5 98.4, and 98.4% identity, respectively. MLSA of the housekeeping genes gyrB, rpoB, and rpoD confirmed that strain IA19T clearly separates from its closest related species. Average nucleotide identity between strains IA19T and P. abietaniphila ATCC 700689T, P. graminis DSM 11363T, P. alkylphenolica KL28T and P. lutea DSM 17257T were 85.3, 80.2, 79.0, and 72.1%, respectively. Growth occurs at 4-37°C and pH 6.5-8. Optimal growth occurs at 28°C, pH 7-8 and up to 2.5% NaCl. Respiratory ubiquinones are Q9 (97%) and Q8 (3%). C16:0 and in summed feature 3 are the main fatty acids. Based on genotypic, phenotypic and chemotaxonomic characteristics, the description of Pseudomonas bohemica sp. nov. has been proposed. The type strain is IA19T (=CECT 9403T = LMG 30182T).

Associated R and D Unit USAL CSIC Salamanca Spain

Institute of Microbiology of the Czech Academy of Sciences Vestec Czechia

Institute of Natural Resources and Agrobiology of Salamanca IRNASA CSIC Salamanca Spain

Microbiology and Genetics Department University of Salamanca Salamanca Spain

Spanish Portuguese Institute for Agricultural Research Salamanca Spain

Zobrazit více v PubMed

Adam Z., Chen Q., Xu R., Diange A. E., Bromfield E. S. P., Tambong J. T. (2015). Draft genome sequence of Pseudomonas simiae strain 2-36, an in vitro antagonist of Rhizoctonia solani and Gaeumannomyces graminis. Genome Announc. 3, e01534–e01514. 10.1128/genomeA.01534-14 PubMed DOI PMC

Adams A. S., Aylward F. O., Adams S. M., Erbilgin N., Aukema B. H., Currie C. R., et al. . (2013). 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. 79, 3468–3475. 10.1128/AEM.00068-13 PubMed DOI PMC

Adams A. S., Currie C. R., Cardoza Y., Klepzig K. D., Raffa K. F. (2009). Effects of symbiotic bacteria and tree chemistry on the growth and reproduction of bark beetle fungal symbionts. Can. J. For. Res. 39, 1133–1147. 10.1139/X09-034 DOI

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

Allen M. S., Becker A. M., Rickards R. W. (1976). The glutarimide antibiotic 9-methylstreptimidone: structure, biogenesis and biological activity. Aust. J. Chem. 29, 673–679. 10.1071/ch9760673 DOI

Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403–410. 10.1016/S0022-2836(05)80360-2 PubMed DOI

Arakawa K., Sugino F., Kodama K., Ishii T., Kinashi H. (2005). Cyclization mechanism for the synthesis of macrocyclic antibiotic lankacidin in Streptomyces rochei. Chem. Biol. 12, 249–256. 10.1016/j.chembiol.2005.01.009 PubMed DOI

Arnam E. B. V., Currie R. C., Clardy J. (2018). Defense contracts: molecular protection in insect-microbe symbioses. Chem. Soc. Rev. 47, 1638–1651. 10.1039/C7CS00340D PubMed DOI

Aziz R. K., Bartels D., Best A. A., DeJongh M., Disz T., Edwards R. A., et al. . (2008). The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75. 10.1186/1471-2164-9-75 PubMed DOI PMC

Balamurugan R., Dekker F. J., Waldmann H. (2005). Design of compound libraries based on natural product scaffolds and protein structure similarity clustering (PSSC). Mol. Biosyst. 1, 36–45. 10.1039/B503623B PubMed DOI

Bauer J. S., Ghequire M. G. K., Nett M., Josten M., Sahl H.-G., De Mot R., et al. . (2015). Biosynthetic origin of the antibiotic Pseudopyronines a and b in Pseudomonas putida BW11M1. ChemBioChem 16, 2491–2497. 10.1002/cbic.201500413 PubMed DOI

Becerra M. C., Eraso A. J., Albesa I. (2003). Comparison of oxidative stress induced by ciprofloxacin and pyoverdin in bacteria and in leukocytes to evaluate toxicity. Luminescence 18, 334–340. 10.1002/bio.742 PubMed DOI

Beyer S., Mayer G., Piepersberg W. (1998). The StrQ protein encoded in the gene cluster for 5′-hydroxystreptomycin of Streptomyces glaucescens GLA.0 is a α- D-glucose-1-phosphate cytidylyltransferase (CDP- D-glucose synthase). Eur. J. Biochem. 258, 1059–1067. 10.1046/j.1432-1327.1998.2581059.x PubMed DOI

Boone C. K., Keefover-Ring K., Mapes A. C., Adams A. S., Bohlmann J., Raffa K. F. (2013). Bacteria associated with a tree-killing insect reduce concentrations of plant defense compounds. J. Chem. Ecol. 39, 1003–1006. 10.1007/s10886-013-0313-0 PubMed DOI

Caffrey P., Lynch S., Flood E., Finnan S., Oliynyk M. (2001). Amphotericin biosynthesis in Streptomyces nodosus: deductions from analysis of polyketide synthase and late genes. Chem. Biol. 8, 713–723. 10.1016/S1074-5521(01)00046-1 PubMed DOI

Cardoza Y. J., Klepzig K. D., Raffa K. F. (2006). Bacteria in oral secretions of an endophytic insect inhibit antagonistic fungi. Ecol. Entomol. 31, 636–645. 10.1111/j.1365-2311.2006.00829.x DOI

Clark L. L., Dajcs J. J., McLean C. H., Bartell J. G., Stroman D. W. (2006). Pseudomonas otitidis sp. nov., isolated from patients with otic infections. Int. J. Syst. Evol. Microbiol. 56, 709–714. 10.1099/ijs.0.63753-0 PubMed DOI

Cragg G. M., Newman D. J. (2009). Biodiversity: a continuing source of novel drug leads. Pure Appl. Chem. 77, 7–24. 10.1351/pac200577010007 DOI

Dias D. A., Urban S., Roessner U. (2012). A historical overview of natural products in drug discovery. Metabolites 2, 303–336. 10.3390/metabo2020303 PubMed DOI PMC

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

Drewry D. H., Macarron R. (2010). Enhancements of screening collections to address areas of unmet medical need: an industry perspective. Curr. Opin. Chem. Biol. 14, 289–298. 10.1016/j.cbpa.2010.03.024 PubMed DOI

Fabryová A., Kostovčík M., Díez-Méndez A., Jiménez-Gómez A., Celador-Lera L., Saati-Santamaría Z., et al. . (2018). On the bright side of a forest pest-the metabolic potential of bark beetles' bacterial associates. Sci. Total Environ. 619–620, 9–17. 10.1016/j.scitotenv.2017.11.074 PubMed DOI

Flórez L. V., Scherlach K., Gaube P., Ross C., Sitte E., Hermes C., et al. . (2017). Antibiotic-producing symbionts dynamically transition between plant pathogenicity and insect-defensive mutualism. Nat. Commun. 8:15172. 10.1038/ncomms15172 PubMed DOI PMC

Frasson D., Opoku M., Picozzi T., Torossi T., Balada S., Smits T. H. M., et al. . (2017). Pseudomonas wadenswilerensis sp. nov. and Pseudomonas reidholzensis sp. nov., two novel species within the Pseudomonas putida group isolated from forest soil. Int. J. Syst. Evol. Microbiol. 67, 2853–2861. 10.1099/ijsem.0.002035 PubMed DOI

Ganne G., Brillet K., Basta B., Roche B., Hoegy F., Gasser V., et al. . (2017). Iron release from the siderophore pyoverdine in Pseudomonas aeruginosa involves three new actors: FpvC, FpvG, and FpvH. ACS Chem. Biol. 12, 1056–1065. 10.1021/acschembio.6b01077 PubMed DOI

García-Fraile P. (2018). Roles of bacteria in the bark beetle holobiont – how do they shape this forest pest? Ann. Appl. Biol. 172, 111–125. 10.1111/aab.12406 DOI

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

Haas D., Keel C. (2003). Regulation of antibiotic production in root-colonizing pseudomonas spp. and relevance for biological control of plant disease. Annu. Rev. Phytopathol. 41, 117–153. 10.1146/annurev.phyto.41.052002.095656 PubMed DOI

Harvey A. L., Edrada-Ebel R., Quinn R. J. (2015). The re-emergence of natural products for drug discovery in the genomics era. Nat. Rev. Drug Discov. 14, 111–129. 10.1038/nrd4510 PubMed DOI

Hennessy R. C., Glaring M. A., Michelsen C. F., Olsson S., Stougaard P. (2015). Draft genome sequence of pseudomonas sp. strain in5 isolated from a greenlandic disease suppressive soil with potent antimicrobial activity. Genome Announc. 3:e01251–15. 10.1128/genomeA.01251-15 PubMed DOI PMC

Hoffman S. J., Outterson K., Røttingen J.-A., Cars O., Clift C., Rizvi Z., et al. . (2015). An international legal framework to address antimicrobial resistance. Bull. World Health Organ. 93, 66–66. 10.2471/BLT.15.152710 PubMed DOI PMC

Hu X., Yu J., Wang C., Chen H. (2014). Cellulolytic bacteria associated with the gut of dendroctonus armandi larvae (coleoptera: curculionidae: scolytinae). Forests 5, 455–465. 10.3390/f5030455 DOI

Ishikawa Y., Tachibana M., Matsui C., Obata R., Umezawa K., Nishiyama S. (2009). Synthesis and biological evaluation on novel analogs of 9-methylstreptimidone, an inhibitor of NF-KB. Bioorg. Med. Chem. Lett. 19, 1726–1728. 10.1016/j.bmcl.2009.01.107 PubMed DOI

Isnansetyo A., Kamei Y. (2009). Bioactive substances produced by marine isolates of Pseudomonas. J. Ind. Microbiol. Biotechnol. 36, 1239–1248. 10.1007/s10295-009-0611-2 PubMed DOI

Kennedy J., Marchesi J. R., Dobson A. D. W. (2007). Metagenomic approaches to exploit the biotechnological potential of the microbial consortia of marine sponges. Appl. Microbiol. Biotechnol. 75, 11–20. 10.1007/s00253-007-0875-2 PubMed DOI

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

Kimura M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111–120. 10.1007/BF01731581 PubMed DOI

Kinzel O., Budzikiewicz H. (1999). Synthesis and biological evaluation of a pyoverdin-β-lactam conjugate: a new type of arginine-specific cross-linking in aqueous solution. J. Pept. Res. 53, 618–625. 10.1034/j.1399-3011.1999.00053.x PubMed DOI

Kinzel O., Tappe R., Gerus I., Budzikiewicz H. (1998). The synthesis and antibacterial activity of two pyoverdin-ampicillin conjugates, entering Pseudomonas aeruginosa via the pyoverdin-mediated iron uptake pathway. J. Antibiot 51, 499–507. 10.7164/antibiotics.51.499 PubMed DOI

Kovacs N. (1956). Identification of Pseudomonas pyocyanea by the oxidase reaction. Nature 178, 703. 10.1038/178703a0 PubMed DOI

Kumar S., Stecher G., Tamura K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874. 10.1093/molbev/msw054 PubMed DOI PMC

Laatsch H., Renneberg B., Hanefeld U., Kellner M., Pudleiner H., Hamprecht G., et al. . (1995). Structure-activity relationships of phenyl- and benzoylpyrroles. Chem. Pharm. Bull. 43, 537–546. 10.1248/cpb.43.537 PubMed DOI

Laine M. H., Karwoski M. T., Raaska L. B., Mattila-Sandholm T.-M. (1996). Antimicrobial activity of Pseudomonas spp. against food poisoning bacteria and moulds. Lett. Appl. Microbiol. 22, 214–218. 10.1111/j.1472-765X.1996.tb01146.x PubMed DOI

Landy M., Warren G. H., Rosenman M. S. B., Colio L. G. (1948). Bacillomycin: an antibiotic from Bacillus subtilis active against pathogenic fungi*. Proc. Soc. Exp. Biol. Med. 67, 539–541. 10.3181/00379727-67-16367 PubMed DOI

Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., et al. . (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948. 10.1093/bioinformatics/btm404 PubMed DOI

Lee X., Azevedo M. D., Armstrong D. J., Banowetz G. M., Reimmann C. (2013). The Pseudomonas aeruginosa antimetabolite L-2-amino-4-methoxy-trans-3-butenoic acid inhibits growth of Erwinia amylovora and acts as a seed germination-arrest factor. Environ. Microbiol. Rep. 5, 83–89. 10.1111/j.1758-2229.2012.00395.x PubMed DOI

Lee X., Fox Á., Sufrin J., Henry H., Majcherczyk P., Haas D., et al. . (2010). Identification of the biosynthetic gene cluster for the pseudomonas aeruginosa antimetabolite l-2-amino-4-methoxy-trans-3-butenoic acid. J. Bacteriol. 192, 4251–4255. 10.1128/JB.00492-10 PubMed DOI PMC

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

Levy S. B., Marshall B. (2004). Antibacterial resistance worldwide: causes, challenges and responses. Nat. Med. N. Y. 10(Suppl. 1), S122–S129. 10.1038/nm1145 PubMed DOI

Maggini V., Presta L., Miceli E., Fondi M., Bosi E., Chiellini C., et al. . (2017). Draft genome sequence of pseudomonas sp. strain ep r1 isolated from echinacea purpurea roots and effective in the growth inhibition of human opportunistic pathogens belonging to the burkholderia cepacia complex. Genome Announc. 5:e00351-17. 10.1128/genomeA.00351-17 PubMed DOI PMC

Marinho P. R., Moreira A. P., Pellegrino F. L., Muricy G., Bastos Mdo C., Santos K. R., et al. . (2009). Marine Pseudomonas putida: a potential source of antimicrobial substances against antibiotic-resistant bacteria. Mem. Inst. Oswaldo Cruz 104, 678–682. 10.1590/S0074-02762009000500002 PubMed DOI

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

Mishra B. B., Tiwari V. K. (2011). Natural products: an evolving role in future drug discovery. Eur. J. Med. Chem. 46, 4769–4807. 10.1016/j.ejmech.2011.07.057 PubMed DOI

Morales-Jiménez J., Zúñiga G., Ramírez-Saad H. C., Hernández-Rodríguez C. (2012). Gut-associated bacteria throughout the life cycle of the bark beetle Dendroctonus rhizophagus thomas and bright (Curculionidae: scolytinae) and their cellulolytic activities. Microb. Ecol. 64, 268–278. 10.1007/s00248-011-9999-0 PubMed DOI

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

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

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

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

Nishanth Kumar S., Aravind S. R., Jacob J., Gopinath G., Lankalapalli R. S., Sreelekha T. T., et al. . (2016). Pseudopyronine B: A potent antimicrobial and anticancer molecule isolated from a pseudomonas mosselii. Front. Microbiol. 7:1307. 10.3389/fmicb.2016.01307 PubMed DOI PMC

Olano C., Gómez C., Pérez M., Palomino M., Pineda-Lucena A., Carbajo R. J., et al. . (2009). Deciphering biosynthesis of the RNA polymerase inhibitor streptolydigin and generation of glycosylated derivatives. Chem. Biol. 16, 1031–1044. 10.1016/j.chembiol.2009.09.015 PubMed DOI

Olorunleke F. E., Kieu Phuong N., Höfte M. (2015). Recent advances in Pseudomonas biocontrol, in Bacteria-Plant Interactions: Advanced Research and Future Trends, eds Murillo J., Vinatzer B. A., Jackson R. W., Arnold D. L. (Poole: Caister Academic Press; ), 167–198.

Onsoyen E., Myrvold R., Dessen A., Thomas D., Walsh T. R. (2010). Treatment of Acinetobacter with Alginate Oligomers and Antibiotics. Patent number: WO2010139956.

Overbeek R., Olson R., Pusch G. D., Olsen G. J., Davis J. J., Disz T., et al. . (2014). The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res. 42, D206–D214. 10.1093/nar/gkt1226 PubMed DOI PMC

Oyaizu H., Komagata K. (1983). Grouping of Pseudomonas species on the basis of cellular fatty acid composition and the quinone system with special reference to the existence of 3-hydroxy fatty acids. J. Gen. Appl. Microbiol. 29, 17–40. 10.2323/jgam.29.17 DOI

Palleroni N. (2005). Genus I Pseudomonas Migula 1894, 237. Bergeys Man. Syst. Bacteriol. 2, 323–378.

Peix A., Ramírez-Bahena M.-H., Velázquez E. (2018). The current status on the taxonomy of Pseudomonas revisited: an update. Infect. Genet. Evol. 57, 106–116. 10.1016/j.meegid.2017.10.026 PubMed DOI

Pérez M., Schleissner C., Fernández R., Rodríguez P., Reyes F., Zuñiga P., et al. . (2016). PM100117 and PM100118, new antitumor macrolides produced by a marine Streptomyces caniferus GUA-06-05-006A. J. Antibiot. 69, 388–394. 10.1038/ja.2015.121 PubMed DOI

Piel J. (2011). Approaches to capturing and designing biologically active small molecules produced by uncultured microbes. Annu. Rev. Microbiol. 65, 431–453. 10.1146/annurev-micro-090110-102805 PubMed DOI

Pierson L. S., Keppenne V. D., Wood D. W. (1994). Phenazine antibiotic biosynthesis in Pseudomonas aureofaciens 30-84 is regulated by PhzR in response to cell density. J. Bacteriol. 176, 3966–3974. 10.1128/jb.176.13.3966-3974.1994 PubMed DOI PMC

Premanandh J., Samara B. S., Mazen A. N. (2016). Race against antimicrobial resistance requires coordinated action – an overview. Front. Microbiol. 6:1536. 10.3389/fmicb.2015.01536 PubMed DOI PMC

Raaijmakers J. M., Weller D. M., Thomashow L. S. (1997). Frequency of antibiotic-producing pseudomonas spp. in natural environments. Appl. Environ. Microbiol. 63, 881–887. PubMed PMC

Ramírez-Bahena M.-H., Cuesta M. J., Flores-Félix J. D., Mulas R., Rivas R., Castro-Pinto J., et al. . (2014). Pseudomonas helmanticensis sp. nov., isolated from forest soil. Int. J. Syst. Evol. Microbiol. 64, 2338–2345. 10.1099/ijs.0.063560-0 PubMed DOI

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

Ravelo A. G., Braun A. E. (2009). Relevancia de los productos naturales en el descubrimiento de nuevos fármacos en el s. XXI. Rev. Real Acad. Cienc. Exactas Físicas Nat. 103, 409–420.

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

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

Rogers J. S., Swofford D. L., Cannatella D. (1998). A fast method for approximating maximum likelihoods of phylogenetic trees from nucleotide sequences. Syst. Biol. 47, 77–89. 10.1080/106351598261049 PubMed DOI

Saito N., Kitame F., Kikuchi M., Ishida N. (1974). Studies on a new antiviral antibiotic, 9-methylstreptimidone. I. Physicochemical and biological properties. J. Antibiot. 27, 206–214. 10.7164/antibiotics.27.206 PubMed DOI

Saitou N., Nei M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425. 10.1093/oxfordjournals.molbev.a040454 PubMed DOI

Sarniguet A., Kraus J., Henkels M. D., Muehlchen A. M., Loper J. E. (1995). The sigma factor sigma s affects antibiotic production and biological control activity of Pseudomonas fluorescens Pf-5. Proc. Natl. Acad. Sci. 92, 12255–12259. 10.1073/pnas.92.26.12255 PubMed DOI PMC

Sasser M. (1990). Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids, MIDI Technical Note 101. Newark, DE: MIDI Inc.

Schnider U., Keel C., Blumer C., Troxler J., Défago G., Haas D. (1995). Amplification of the housekeeping sigma factor in Pseudomonas fluorescens CHA0 enhances antibiotic production and improves biocontrol abilities. J. Bacteriol. 177, 5387–5392. 10.1128/jb.177.18.5387-5392.1995 PubMed DOI PMC

Sedkova N., Tao L., Rouvière P. E., Cheng Q. (2005). Diversity of carotenoid synthesis gene clusters from environmental enterobacteriaceae strains. Appl. Environ. Microbiol. 71, 8141–8146. 10.1128/AEM.71.12.8141-8146.2005 PubMed DOI PMC

Six D. L. (2012). Ecological and evolutionary determinants of bark beetle —fungus symbioses. Insects 3, 339–366. 10.3390/insects3010339 PubMed DOI PMC

Stintzi A., Cornelis P., Hohnadel D., Meyer J.-M., Dean C., Poole K., et al. . (1996). Novel pyoverdine biosynthesis gene(s) of Pseudomonas aeruginosa PAO. Microbiology 142, 1181–1190. 10.1099/13500872-142-5-1181 PubMed DOI

Therrien J., Mason C. J., Cale J. A., Adams A., Aukema B. H., Currie C. R., et al. . (2015). Bacteria influence mountain pine beetle brood development through interactions with symbiotic and antagonistic fungi: implications for climate-driven host range expansion. Oecologia 179, 467–485. 10.1007/s00442-015-3356-9 PubMed DOI

Thompson J. D., Higgins D. G., Gibson T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680. 10.1093/nar/22.22.4673 PubMed DOI PMC

Tindall B. J. (1990a). A comparative study of the lipid composition of halobacterium saccharovorum from various sources. Syst. Appl. Microbiol. 13, 128–130. 10.1016/S0723-2020(11)80158-X DOI

Tindall B. J. (1990b). Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol. Lett. 66, 199–202. 10.1111/j.1574-6968.1990.tb03996.x DOI

Tisdale M. J. (1980). The effect of the methionine antagonist l-2-amino-4-methoxy-trans-3-butenoic acid on the growth and metabolism of walker carcinosarcoma in vitro. Biochem. Pharmacol. 29, 501–508. 10.1016/0006-2952(80)90369-X PubMed DOI

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

Verani A., Sironi F., Siccardi A. G., Lusso P., Vercelli D. (2002). Inhibition of CXCR4-tropic HIV-1 infection by lipopolysaccharide: evidence of different mechanisms in macrophages and T Lymphocytes. J. Immunol. 168, 6388–6395. 10.4049/jimmunol.168.12.6388 PubMed DOI

Vida C., de Vicente A., Cazorla F. M. (2017). Draft genome sequence of the rhizobacterium Pseudomonas chlororaphis PCL1601, displaying biocontrol against soilborne phytopathogens. Genome Announc. 5, e00130–e00117. 10.1128/genomeA.00130-17 PubMed DOI PMC

Weber T., Blin K., Duddela S., Krug D., Kim H. U., Bruccoleri R., et al. . (2015). AntiSMASH 3.0—a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res. 43, W237–W243. 10.1093/nar/gkv437 PubMed DOI PMC

Wemheuer F., Hollensteiner J., Poehlein A., Granzow S., Daniel R., Vidal S., et al. . (2017). Draft genome sequence of pseudomonas putida strain GM4FR, an endophytic bacterium isolated from Festuca rubra L. Genome Announc. 5, e00086–e00017. 10.1128/genomeA.00086-17 PubMed DOI PMC

Xiao Y.-P., Hui W., Wang Q., Roh S. W., Shi X.-Q., Shi J.-H., et al. . (2009). Pseudomonas caeni sp. nov., a denitrifying bacterium isolated from the sludge of an anaerobic ammonium-oxidizing bioreactor. Int. J. Syst. Evol. Microbiol. 59, 2594–2598. 10.1099/ijs.0.005108-0 PubMed DOI

Xu L., Lou Q., Cheng C., Lu M., Sun J. (2015). Gut-associated bacteria of dendroctonus valens and their involvement in verbenone production. Microb. Ecol. 70, 1012–1023. 10.1007/s00248-015-0625-4 PubMed DOI

Xu L.-T., Lu M., Sun J.-H. (2016). Invasive bark beetle-associated microbes degrade a host defensive monoterpene. Insect Sci. 23, 183–190. 10.1111/1744-7917.12255 PubMed DOI

Yamaguchi M., Park H. J., Ishizuka S., Omata K., Hirama M. (1995). Chemistry and antimicrobial activity of caryoynencins analogs. J. Med. Chem. 38, 5015–5022. 10.1021/jm00026a008 PubMed DOI

Zerbino D. R., Birney E. (2008). Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821–829. 10.1101/gr.074492.107 PubMed DOI PMC

Zhuang Y. P., Chen B., Chu J., Zhang S. (2006). Medium optimization for meilingmycin production by Streptomyces nanchangensis using response surface methodology. Process Biochem. 41, 405–409. 10.1016/j.procbio.2005.07.004 DOI

New insight into the bark beetle ips typographus bacteriome reveals unexplored diversity potentially beneficial to the host

Comparative Genomics of the Genus Pseudomonas Reveals Host- and Environment-Specific Evolution

A New Perspective of Pseudomonas-Host Interactions: Distribution and Potential Ecological Functions of the Genus Pseudomonas within the Bark Beetle Holobiont

Genome Analysis and Genomic Comparison of the Novel Species Arthrobacter ipsi Reveal Its Potential Protective Role in Its Bark Beetle Host

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