Unravelling the gut bacteriome of Ips (Coleoptera: Curculionidae: Scolytinae): identifying core bacterial assemblage and their ecological relevance

. 2020 Oct 29 ; 10 (1) : 18572. [epub] 20201029

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33122700
Odkazy

PubMed 33122700
PubMed Central PMC7596566
DOI 10.1038/s41598-020-75203-5
PII: 10.1038/s41598-020-75203-5
Knihovny.cz E-zdroje

Bark beetles often serve as forest damaging agents, causing landscape-level mortality. Understanding the biology and ecology of beetles are important for both, gathering knowledge about important forest insects and forest protection. Knowledge about the bark beetle gut-associated bacteria is one of the crucial yet surprisingly neglected areas of research with European tree-killing bark beetles. Hence, in this study, we survey the gut bacteriome from five Ips and one non-Ips bark beetles from Scolytinae. Results reveal 69 core bacterial genera among five Ips beetles that may perform conserved functions within the bark beetle holobiont. The most abundant bacterial genera from different bark beetle gut include Erwinia, Sodalis, Serratia, Tyzzerella, Raoultella, Rahnella, Wolbachia, Spiroplasma, Vibrio, and Pseudoxanthomonas. Notable differences in gut-associated bacterial community richness and diversity among the beetle species are observed. Furthermore, the impact of sampling location on the overall bark beetle gut bacterial community assemblage is also documented, which warrants further investigations. Nevertheless, our data expanded the current knowledge about core gut bacterial communities in Ips bark beetles and their putative function such as cellulose degradation, nitrogen fixation, detoxification of defensive plant compounds, and inhibition of pathogens, which could serve as a basis for further metatranscriptomics and metaproteomics investigations.

Zobrazit více v PubMed

Anderegg WR, Kane JM, Anderegg LD. Consequences of widespread tree mortality triggered by drought and temperature stress. Nat. Clim. Chang. 2013;3:30–36. doi: 10.1038/nclimate1635. DOI

Huang J, et al. Tree defence and bark beetles in a drying world: Carbon partitioning, functioning and modelling. New Phytol. 2020;225:26–36. doi: 10.1111/nph.16173. PubMed DOI

Kautz M, Meddens AJ, Hall RJ, Arneth A. Biotic disturbances in Northern Hemisphere forests—A synthesis of recent data, uncertainties and implications for forest monitoring and modelling. Glob. Ecol. Biogeogr. 2017;26:533–552. doi: 10.1111/geb.12558. DOI

Netherer S, et al. Do water-limiting conditions predispose N orway spruce to bark beetle attack? New Phytol. 2015;205:1128–1141. doi: 10.1111/nph.13166. PubMed DOI PMC

Seybold SJ, Huber DP, Lee JC, Graves AD, Bohlmann J. Pine monoterpenes and pine bark beetles: A marriage of convenience for defense and chemical communication. Phytochem. Rev. 2006;5:143–178. doi: 10.1007/s11101-006-9002-8. DOI

Raffa KF, Smalley EB. Interaction of pre-attack and induced monoterpene concentrations in host conifer defense against bark beetle-fungal complexes. Oecologia. 1995;102:285–295. doi: 10.1007/BF00329795. PubMed DOI

Reid ML, Purcell J. Condition-dependent tolerance of monoterpenes in an insect herbivore. Arthropod-Plant Interact. 2011;5:331–337. doi: 10.1007/s11829-011-9137-4. DOI

Erbilgin N, Krokene P, Christiansen E, Zeneli G, Gershenzon J. Exogenous application of methyl jasmonate elicits defenses in Norway spruce (Picea abies) and reduces host colonization by the bark beetle Ips typographus. Oecologia. 2006;148:426–436. doi: 10.1007/s00442-006-0394-3. PubMed DOI

Hayes JL, Strom BL. 4-Allylanisole as an inhibitor of bark beetle (Coleoptera: Scolytidae) aggregation. J. Econ. Entomol. 1994;87:1586–1594. doi: 10.1093/jee/87.6.1586. DOI

Franceschi VR, Krokene P, Christiansen E, Krekling T. Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol. 2005;167:353–376. doi: 10.1111/j.1469-8137.2005.01436.x. PubMed DOI

Zhao T, Borg-Karlson A-K, Erbilgin N, Krokene P. Host resistance elicited by methyl jasmonate reduces emission of aggregation pheromones by the spruce bark beetle, Ips typographus. Oecologia. 2011;167:691–699. doi: 10.1007/s00442-011-2017-x. PubMed DOI

12Schmidt, A. et al. In Chemical Ecology and Phytochemistry in Forest Ecosystems (ed Romeo, J. T.) 1–28 (Elsevier, Amsterdam, 2005).

Keeling CI, Bohlmann J. Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol. 2006;170:657–675. doi: 10.1111/j.1469-8137.2006.01716.x. PubMed DOI

Despres L, David J-P, Gallet C. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 2007;22:298–307. doi: 10.1016/j.tree.2007.02.010. PubMed DOI

Raffa, K., Andersson, M. N. & Schlyter, F. In Advances in Insect Physiology, Vol. 50 (ed Blomquist Claus Tittiger, G.J.) 1–74 (Elsevier, Amsterdam, 2016).

Adams AS, et al. Mountain pine beetles colonizing historical and naive 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

Six DL. Ecological and evolutionary determinants of bark beetle—fungus symbioses. Insects. 2012;3:339–366. doi: 10.3390/insects3010339. PubMed DOI PMC

Raffa KF. Terpenes tell different tales at different scales: Glimpses into the chemical ecology of conifer-bark beetle-microbial interactions. J. Chem. Ecol. 2014;40:1–20. doi: 10.1007/s10886-013-0368-y. PubMed DOI

Douglas AE. Multiorganismal insects: Diversity and function of resident microorganisms. Annu. Rev. Entomol. 2015;60:17–34. doi: 10.1146/annurev-ento-010814-020822. PubMed DOI PMC

Douglas AE. The microbial dimension in insect nutritional ecology. Funct. Ecol. 2009;23:38–47. doi: 10.1111/j.1365-2435.2008.01442.x. DOI

Ceja-Navarro JA, et al. Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee. Nat. Commun. 2015;6:7618. doi: 10.1038/ncomms8618. PubMed DOI PMC

Welte CU, et al. Plasmids from the gut microbiome of cabbage root fly larvae encode SaxA that catalyses the conversion of the plant toxin 2-phenylethyl isothiocyanate. Environ. Microbiol. 2016;18:1379–1390. doi: 10.1111/1462-2920.12997. PubMed DOI

Hammer TJ, Bowers MD. Gut microbes may facilitate insect herbivory of chemically defended plants. Oecologia. 2015;179:1–14. doi: 10.1007/s00442-015-3327-1. PubMed DOI

Bakkali F, Averbeck S, Averbeck D, Idaomar M. Biological effects of essential oils—A review. Food Chem. Toxicol. 2008;46:446–475. doi: 10.1016/j.fct.2007.09.106. PubMed DOI

Mithöfer A, Boland W. Plant defense against herbivores: Chemical aspects. Annu. Rev. Plant Biol. 2012;63:431–450. doi: 10.1146/annurev-arplant-042110-103854. PubMed DOI

Douglas A. Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera. Annu. Rev. Entomol. 1998;43:17–37. doi: 10.1146/annurev.ento.43.1.17. PubMed DOI

Ayres MP, Wilkens RT, Ruel JJ, Lombardero MJ, Vallery E. Nitrogen budgets of phloem-feeding bark beetles with and without symbiotic fungi. Ecology. 2000;81:2198–2210. doi: 10.1890/0012-9658(2000)081[2198:NBOPFB]2.0.CO;2. DOI

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

Cardoza YJ, Moser JC, Klepzig KD, Raffa KF. Multipartite symbioses among fungi, mites, nematodes, and the spruce beetle, Dendroctonus rufipennis. Environ. Entomol. 2008;37:956–963. doi: 10.1093/ee/37.4.956. PubMed DOI

Therrien J, et al. Bacteria influence mountain pine beetle brood development through interactions with symbiotic and antagonistic fungi: Implications for climate-driven host range expansion. Oecologia. 2015;179:467–485. doi: 10.1007/s00442-015-3356-9. PubMed DOI

Morales-Jiménez J, Zúñiga G, Ramírez-Saad HC, 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

Delalibera I, Jr, Handelsman J, Raffa KF. Contrasts in cellulolytic activities of gut microorganisms between the wood borer, Saperda vestita (Coleoptera: Cerambycidae), and the bark beetles, Ips pini and Dendroctonus frontalis (Coleoptera: Curculionidae) Environ. Entomol. 2005;34:541–547. doi: 10.1603/0046-225X-34.3.541. DOI

Hu X, Yu J, Wang C, Chen H. Cellulolytic bacteria associated with the gut of Dendroctonus armandi larvae (Coleoptera: Curculionidae: Scolytinae) Forests. 2014;5:455–465. doi: 10.3390/f5030455. DOI

Menéndez E, et al. 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

Boone CK, et al. 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

Xu LT, Lu M, Sun JH. Invasive bark beetle-associated microbes degrade a host defensive monoterpene. Insect Sci. 2016;23:183–190. doi: 10.1111/1744-7917.12255. PubMed DOI

Berasategui A, et al. Gut microbiota of the pine weevil degrades conifer diterpenes and increases insect fitness. Mol. Ecol. 2017;26:4099–4110. doi: 10.1111/mec.14186. PubMed DOI

Engl T, Kaltenpoth M. Influence of microbial symbionts on insect pheromones. Nat. Prod. Rep. 2018;35:386–397. doi: 10.1039/C7NP00068E. PubMed DOI

Howe M, Keefover-Ring K, Raffa KF. Pine engravers carry bacterial communities whose members reduce concentrations of host monoterpenes with variable degrees of redundancy, specificity, and capability. Environ. Entomol. 2018;47:638–645. doi: 10.1093/ee/nvy032. PubMed DOI

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

Skrodenytė-Arbačiauskienė V, Radžiutė S, Stunžėnas V, Būda V. Erwiniatypographi 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

Smith DJ, Park J, Tiedje JM, Mohn WW. A large gene cluster in Burkholderia xenovorans encoding abietane diterpenoid catabolism. J. Bacteriol. 2007;189:6195–6204. doi: 10.1128/JB.00179-07. PubMed DOI PMC

Martin VJ, Mohn WW. Genetic investigation of the catabolic pathway for degradation of abietane diterpenoids by Pseudomonas abietaniphila BKME-9. J. Bacteriol. 2000;182:3784–3793. doi: 10.1128/JB.182.13.3784-3793.2000. PubMed DOI PMC

Muratoğlu H, Sezen K, Demirbağ Z. Determination and pathogenicity of the bacterial flora associated with the spruce bark beetle, Ips typographus (L.) (Coleoptera: Curculionidae: Scolytinae) Turk. J. Biol. 2011;35:9–20.

Skrodenytė-Arbačiauskienė V, Būda V, Radžiutė S, Stunžėnas V. Myrcene-resistant bacteria isolated from the gut of phytophagous insect Ips typographus. Ekologija. 2006;4:1–6.

Sevim A, Gökçe C, Erbaş Z, Özkan F. Bacteria from Ips sexdentatus (Coleoptera: Curculionidae) and their biocontrol potential. J. Basic Microbiol. 2012;52:695–704. doi: 10.1002/jobm.201100564. PubMed DOI

Vasanthakumar A, et al. Composition of the bacterial community in the gut of the pine engraver, Ips pini (Say) (Coloptera) colonizing red pine. Symbiosos. 2007;43:97–104.

48Grégoire, J.-C. & Evans, H. In Bark and Wood Boring Insects in Living Trees in Europe, a Synthesis (eds Lieutier, F., Day, K.R., Battisti, A., Grégoire, J.-C., Evans, H.F.) 19–37 (Springer, Berlin, 2007).

Kolk, A., Starzyk, J., Kinelski, S. & Dzwonkowski, R. Atlas of Forest Insect Pests. (MULTICO Publishing House Ltd., 1996).

Davydenko K, Vasaitis R, Menkis A. Fungi associated with Ips acuminatus (Coleoptera: Curculionidae) in Ukraine with a special emphasis on pathogenicity of ophiostomatoid species. Eur. J. Entomol. 2017;114:77–85. doi: 10.14411/eje.2017.011. DOI

Fettig, C. J. & Hilszczański, J. In Bark Beetles: Biology and Ecology of Native and Invasive Species (eds Vega, F.E, Hofstetter, R.W.) 555–584 (Springer, Berlin, 2015).

Knížek, M., Liška, J. & Modlinger, R. Výskyt lesních škodlivých činitelů v roce 2015 a jejich očekávaný stav v roce 2016. Strnady, VÚLHM, Zpravodaj ochrany lesa (2016).

Villari C, et al. Nutritional and pathogenic fungi associated with the pine engraver beetle trigger comparable defenses in Scots pine. Tree Physiol. 2012;32:867–879. doi: 10.1093/treephys/tps056. PubMed DOI

Wermelinger B, Rigling A, Schneider Mathis D, Dobbertin M. Assessing the role of bark-and wood-boring insects in the decline of Scots pine (Pinus sylvestris) in the Swiss Rhone valley. Ecol. Entomol. 2008;33:239–249. doi: 10.1111/j.1365-2311.2007.00960.x. DOI

Pineau X, Bourguignon M, Jactel H, Lieutier F, Sallé A. Pyrrhic victory for bark beetles: Successful standing tree colonization triggers strong intraspecific competition for offspring of Ips sexdentatus. For. Ecol. Manag. 2017;399:188–196. doi: 10.1016/j.foreco.2017.05.044. DOI

Engel P, Moran NA. The gut microbiota of insects–diversity in structure and function. FEMS Microbiol. Rev. 2013;37:699–735. doi: 10.1111/1574-6976.12025. PubMed DOI

Hernández-García JA, Briones-Roblero CI, Rivera-Orduña FN, Zúñiga G. Revealing the gut bacteriome of Dendroctonus bark beetles (Curculionidae: Scolytinae): Diversity, core members and co-evolutionary patterns. Sci. Rep. 2017;7:1–12. doi: 10.1038/s41598-017-14031-6. PubMed DOI PMC

Morrison M, Miron J. Adhesion to cellulose by Ruminococcus albus: A combination of cellulosomes and Pil-proteins? FEMS Microbiol. Lett. 2000;185:109–115. doi: 10.1111/j.1574-6968.2000.tb09047.x. PubMed DOI

Fabryová A, et al. On the bright side of a forest pest-the metabolic potential of bark beetles' bacterial associates. Sci. Total Environ. 2018;619:9–17. doi: 10.1016/j.scitotenv.2017.11.074. PubMed DOI

Briones-Roblero CI, et al. Structure and dynamics of the gut bacterial microbiota of the bark beetle, Dendroctonus rhizophagus (Curculionidae: Scolytinae) across their life stages. PLoS ONE. 2017;12:e0175470. doi: 10.1371/journal.pone.0175470. PubMed DOI PMC

Sudachkova N, Milyutina I, Romanova L, Semenova G. The annual dynamics of reserve compounds and hydrolitic enzymes activity in the tissues of Pinus sylvestris L. and Larix sibirica Ledeb.: The metabolism of reserve compounds in the tissues of Siberian conifers. Eurasian J. For. Res. 2004;7:1–10.

Horne I, Haritos VS, Oakeshott JG. Comparative and functional genomics of lipases in holometabolous insects. Insect Biochem. Mol. Biol. 2009;39:547–567. doi: 10.1016/j.ibmb.2009.06.002. PubMed DOI

Arrese EL, Soulages JL. Insect fat body: Energy, metabolism, and regulation. Annu. Rev. Entomol. 2010;55:207–225. doi: 10.1146/annurev-ento-112408-085356. PubMed DOI PMC

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

Morales-Jiménez J, et al. 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

Morales-Jiménez J, Zúñiga G, Villa-Tanaca L, Hernández-Rodríguez C. Bacterial community and nitrogen fixation in the red turpentine beetle, Dendroctonus valens LeConte (Coleoptera: Curculionidae: Scolytinae) Microb. Ecol. 2009;58:879–891. doi: 10.1007/s00248-009-9548-2. PubMed DOI

Menna PM, Hungria M. Phylogeny of nodulation and nitrogen-fixation genes in Bradyrhizobium: Supporting evidence for the theory of monophyletic origin, and spread and maintenance by both horizontal and vertical transfer. Int. J. Syst. Evol. Microbiol. 2011;61:3052–3067. doi: 10.1099/ijs.0.028803-0. PubMed DOI

Chen W-M, et al. Legume symbiotic nitrogen fixation byβ-proteobacteria is widespread in nature. J. Bacteriol. 2003;185:7266–7272. doi: 10.1128/JB.185.24.7266-7272.2003. PubMed DOI PMC

Gurevitch J, Scheiner SM, Fox GA. The Ecology of Plants. Sunderland: Sinauer Associates; 2002.

Gibson CM, Hunter MS. Extraordinarily widespread and fantastically complex: Comparative biology of endosymbiotic bacterial and fungal mutualists of insects. Ecol. Lett. 2010;13:223–234. doi: 10.1111/j.1461-0248.2009.01416.x. PubMed DOI

Six DL, Bentz BJ. Fungi associated with the North American spruce beetle, Dendroctonus rufipennis. Can. J. For. Res. 2003;33:1815–1820. doi: 10.1139/x03-107. DOI

Naik PR, Sakthivel N. Functional characterization of a novel hydrocarbonoclastic Pseudomonas sp. strain PUP6 with plant-growth-promoting traits and antifungal potential. Res. Microbiol. 2006;157:538–546. doi: 10.1016/j.resmic.2005.11.009. PubMed DOI

Park G-K, Lim J-H, Kim S-D, Shim S-H. Elucidation of antifungal metabolites produced by Pseudomonas aurantiaca IB5-10 with broad-spectrum antifungal activity. J. Microbiol. Biotechnol. 2012;22:326–330. doi: 10.4014/jmb.1106.06042. PubMed DOI

Elsden SR, Hilton MG, Waller JM. The end products of the metabolism of aromatic amino acids by Clostridia. Arch. Microbiol. 1976;107:283–288. doi: 10.1007/BF00425340. PubMed DOI

Byers J, Birgersson G. Pheromone production in a bark beetle independent of myrcene precursor in host pine species. Naturwissenschaften. 1990;77:385–387. doi: 10.1007/BF01135739. DOI

Blomquist GJ, et al. Pheromone production in bark beetles. Insect Biochem. Mol. Biol. 2010;40:699–712. doi: 10.1016/j.ibmb.2010.07.013. PubMed DOI

Cao Q, et al. Effect of oxygen on verbenone conversion from cis-verbenol by gut facultative anaerobes of Dendroctonus valens. Front. Microbiol. 2018;9:464. doi: 10.3389/fmicb.2018.00464. PubMed DOI PMC

Wang Y, Zhang Y. Investigation of gut-associated bacteria in Tenebrio molitor (Coleoptera: Tenebrionidae) larvae using culture-dependent and DGGE methods. Ann. Entomol. Soc. Am. 2015;108:941–949. doi: 10.1093/aesa/sav079. DOI

Durand A-A, et al. Surveying the endomicrobiome and ectomicrobiome of bark beetles: The case of Dendroctonus simplex. Sci. Rep. 2015;5:17190. doi: 10.1038/srep17190. PubMed DOI PMC

Scott JJ, et al. Bacterial protection of beetle-fungus mutualism. Science. 2008;322:63–63. doi: 10.1126/science.1160423. PubMed DOI PMC

Dale C, Maudlin I. Sodalis gen. nov. and Sodalis glossinidius sp. nov., a microaerophilic secondary endosymbiont of the tsetse fly Glossina morsitans morsitans. Int. J. Syst. Evol. Microbiol. 1999;49:267–275. doi: 10.1099/00207713-49-1-267. PubMed DOI

Santos-Garcia D, Silva FJ, Morin S, Dettner K, Kuechler SM. The all-rounder Sodalis: A new bacteriome-associated endosymbiont of the lygaeoid bug Henestaris halophilus (Heteroptera: Henestarinae) and a critical examination of its evolution. Genome Biol. Evol. 2017;9:2893–2910. doi: 10.1093/gbe/evx202. PubMed DOI PMC

Lawson ET, Mousseau TA, Klaper R, Hunter MD, Werren JH. Rickettsia associated with male-killing in a buprestid beetle. Heredity. 2001;86:497–505. doi: 10.1046/j.1365-2540.2001.00848.x. PubMed DOI

Hurst G, Jiggins FM. Male-killing bacteria in insects: Mechanisms, incidence, and implications. Emerg. Infect. Dis. 2000;6:329. doi: 10.3201/eid0604.000402. PubMed DOI PMC

Stackebrandt, E. & Schumann, P. In The Prokaryotes: Actinobacteria (eds Rosenberg, E. et al.) 163–184 (Springer, Berlin, 2014).

Pfeffer, A. Fauna ČSR. Svazek 6: Kůrovci-Scolytoidea. Řád: Brouci-Coleoptera. (Nakladatelství Československé akadmie věd, 1955).

Pfeffer, A. Zentral-und westpaläarktische Borken-und Kernkäfer:(Coloptera: Scolytidae, Platypodidae). (Pro Entomologia, 1995).

Nunberg, M. Klucze do rozpoznawania owadów Polski [Keys for the identification of Polish Insects]. Część XIX. Chrząszcze–Coleoptera, Korniki–Scolytidae, Wyrynniki–Platypodidae, PWN, Warszawa-Wroclaw. Zeszyt, 99–100 (1981).

Chakraborty A, et al. Core mycobiome and their ecological relevance in the gut of five ips bark beetles (Coleoptera: Curculionidae: Scolytinae) Front. Microbiol. 2020;11:2134. PubMed PMC

Klindworth A, et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 2013;41:e1–e1. doi: 10.1093/nar/gks808. PubMed DOI PMC

Magoč T, Salzberg SL. FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics. 2011;27:2957–2963. doi: 10.1093/bioinformatics/btr507. PubMed DOI PMC

Bokulich NA, et al. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat. Methods. 2013;10:57–59. doi: 10.1038/nmeth.2276. PubMed DOI PMC

Caporaso JG, et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods. 2010;7:335. doi: 10.1038/nmeth.f.303. PubMed DOI PMC

Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27:2194–2200. doi: 10.1093/bioinformatics/btr381. PubMed DOI PMC

Edgar RC. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nat. Methods. 2013;10:996. doi: 10.1038/nmeth.2604. PubMed DOI

Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 2007;73:5261–5267. doi: 10.1128/AEM.00062-07. PubMed DOI PMC

Quast C, et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 2012;41:D590–D596. doi: 10.1093/nar/gks1219. PubMed DOI PMC

Edgar RC. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797. doi: 10.1093/nar/gkh340. PubMed DOI PMC

Chao A, Lee SM, Chen TC. A generalized Good's nonparametric coverage estimator. Chin. J. Math. 1988;16:189–199.

Magurran AE. Ecological Diversity and its Measurement. Princeton: Princeton University Press; 1988.

Team, R. C. R: A Language and Environment for Statistical Computing (Version 2.15. 3) [Computer software] (R Foundation for Statistical Computing, Vienna, 2013).

Oksanen, J. et al. Vegan: community ecology package. R package version 1.17–4. https://CRAN.R-project.org/package=vegan (2010).

Lozupone CA, Hamady M, Kelley ST, Knight R. Quantitative and qualitative β diversity measures lead to different insights into factors that structure microbial communities. Appl. Environ. Microbiol. 2007;73:1576–1585. doi: 10.1128/AEM.01996-06. PubMed DOI PMC

Clarke KR. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 1993;18:117–143. doi: 10.1111/j.1442-9993.1993.tb00438.x. DOI

Cai L. Multi-response permutation procedure as an alternative to the analysis of variance: An SPSS implementation. Behav. Res. Methods. 2006;38:51–59. doi: 10.3758/BF03192749. PubMed DOI

Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral. Ecol. 2001;26:32–46.

Excoffier L, Smouse PE, Quattro JM. Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics. 1992;131:479–491. PubMed PMC

D’Argenio V, Casaburi G, Precone V, Salvatore F. Comparative metagenomic analysis of human gut microbiome composition using two different bioinformatic pipelines. Biomed. Res. Int. 2014;325340:1–10. doi: 10.1155/2014/325340. PubMed DOI PMC

Paulson JN, Pop M, Bravo HC. Metastats: An improved statistical method for analysis of metagenomic data. Genome Biol. 2011;12:P17. doi: 10.1186/1465-6906-12-S1-P17. PubMed DOI

Segata N, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60. doi: 10.1186/gb-2011-12-6-r60. PubMed DOI PMC

Douglas, G. M., Beiko, R. G. & Langille, M. G. In Microbiome Analysis: Methods and Protocols. (eds Beiko, R. G., Hsiao, W. & Parkinson, J.) 169–177 (Springer, Berlin, 2018).

Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 2012;40:D109–D114. doi: 10.1093/nar/gkr988. PubMed DOI PMC

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Comparative metagenomic study unveils new insights on bacterial communities in two pine-feeding Ips beetles (Coleoptera: Curculionidae: Scolytinae)

. 2024 ; 15 () : 1400894. [epub] 20241009

Insights into the Detoxification of Spruce Monoterpenes by the Eurasian Spruce Bark Beetle

. 2024 Sep 23 ; 25 (18) : . [epub] 20240923

Comparative gut proteomics study revealing adaptive physiology of Eurasian spruce bark beetle, Ips typographus (Coleoptera: Scolytinae)

. 2023 ; 14 () : 1157455. [epub] 20231121

The gut microbiome mediates adaptation to scarce food in Coleoptera

. 2023 Nov 13 ; 18 (1) : 80. [epub] 20231113

Genome and transcriptome of Ips nitidus provide insights into high-altitude hypoxia adaptation and symbiosis

. 2023 Oct 20 ; 26 (10) : 107793. [epub] 20230830

Impact of transgenerational host switch on gut bacterial assemblage in generalist pest, Spodoptera littoralis (Lepidoptera: Noctuidae)

. 2023 ; 14 () : 1172601. [epub] 20230713

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

. 2023 Jun 09 ; 18 (1) : 53. [epub] 20230609

Impact of Wood Age on Termite Microbial Assemblages

. 2023 May 31 ; 89 (5) : e0036123. [epub] 20230417

Epigenetic regulations as drivers of insecticide resistance and resilience to climate change in arthropod pests

. 2022 ; 13 () : 1044980. [epub] 20230106

Molecular Rationale of Insect-Microbes Symbiosis-From Insect Behaviour to Mechanism

. 2021 Nov 24 ; 9 (12) : . [epub] 20211124

Reference Gene Selection for Normalizing Gene Expression in Ips Sexdentatus (Coleoptera: Curculionidae: Scolytinae) Under Different Experimental Conditions

. 2021 ; 12 () : 752768. [epub] 20211027

A highly-contiguous genome assembly of the Eurasian spruce bark beetle, Ips typographus, provides insight into a major forest pest

. 2021 Sep 09 ; 4 (1) : 1059. [epub] 20210909

Interactions among Norway spruce, the bark beetle Ips typographus and its fungal symbionts in times of drought

. 2021 ; 94 (3) : 591-614. [epub] 20210222

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

. 2021 Feb 19 ; 10 (2) : . [epub] 20210219

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...