in

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

  • 1.

    Anderegg, W. R., Kane, J. M. & Anderegg, L. D. Consequences of widespread tree mortality triggered by drought and temperature stress. Nat. Clim. Chang. 3, 30–36 (2013).

    ADS  Article  Google Scholar 

  • 2.

    Huang, J. et al. Tree defence and bark beetles in a drying world: Carbon partitioning, functioning and modelling. New Phytol. 225, 26–36 (2020).

    PubMed  Article  PubMed Central  Google Scholar 

  • 3.

    Kautz, M., Meddens, A. J., Hall, R. J. & Arneth, A. Biotic disturbances in Northern Hemisphere forests—A synthesis of recent data, uncertainties and implications for forest monitoring and modelling. Glob. Ecol. Biogeogr. 26, 533–552 (2017).

    Article  Google Scholar 

  • 4.

    Netherer, S. et al. Do water-limiting conditions predispose N orway spruce to bark beetle attack?. New Phytol. 205, 1128–1141 (2015).

    PubMed  Article  PubMed Central  Google Scholar 

  • 5.

    Seybold, S. J., Huber, D. P., Lee, J. C., Graves, A. D. & Bohlmann, J. Pine monoterpenes and pine bark beetles: A marriage of convenience for defense and chemical communication. Phytochem. Rev. 5, 143–178 (2006).

    CAS  Article  Google Scholar 

  • 6.

    Raffa, K. F. & Smalley, E. B. Interaction of pre-attack and induced monoterpene concentrations in host conifer defense against bark beetle-fungal complexes. Oecologia 102, 285–295 (1995).

    ADS  PubMed  Article  PubMed Central  Google Scholar 

  • 7.

    Reid, M. L. & Purcell, J. Condition-dependent tolerance of monoterpenes in an insect herbivore. Arthropod-Plant Interact. 5, 331–337 (2011).

    Article  Google Scholar 

  • 8.

    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 148, 426–436 (2006).

    ADS  PubMed  Article  PubMed Central  Google Scholar 

  • 9.

    Hayes, J. L. & Strom, B. L. 4-Allylanisole as an inhibitor of bark beetle (Coleoptera: Scolytidae) aggregation. J. Econ. Entomol. 87, 1586–1594 (1994).

    CAS  Article  Google Scholar 

  • 10.

    Franceschi, V. R., Krokene, P., Christiansen, E. & Krekling, T. Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol. 167, 353–376 (2005).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 11.

    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 167, 691–699 (2011).

    ADS  PubMed  Article  PubMed Central  Google Scholar 

  • 12.

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

  • 13.

    Keeling, C. I. & Bohlmann, J. Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol. 170, 657–675 (2006).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 14.

    Despres, L., David, J.-P. & Gallet, C. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 22, 298–307 (2007).

    PubMed  Article  PubMed Central  Google Scholar 

  • 15.

    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).

  • 16.

    Adams, A. S. 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. 79, 3468–3475 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 17.

    Six, D. L. Ecological and evolutionary determinants of bark beetle—fungus symbioses. Insects 3, 339–366 (2012).

    PubMed  PubMed Central  Article  Google Scholar 

  • 18.

    Raffa, K. F. Terpenes tell different tales at different scales: Glimpses into the chemical ecology of conifer-bark beetle-microbial interactions. J. Chem. Ecol. 40, 1–20 (2014).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 19.

    Douglas, A. E. Multiorganismal insects: Diversity and function of resident microorganisms. Annu. Rev. Entomol. 60, 17–34 (2015).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 20.

    Douglas, A. E. The microbial dimension in insect nutritional ecology. Funct. Ecol. 23, 38–47 (2009).

    Article  Google Scholar 

  • 21.

    Ceja-Navarro, J. A. et al. Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee. Nat. Commun. 6, 7618 (2015).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 22.

    Welte, C. U. 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. 18, 1379–1390 (2016).

    CAS  PubMed  Article  Google Scholar 

  • 23.

    Hammer, T. J. & Bowers, M. D. Gut microbes may facilitate insect herbivory of chemically defended plants. Oecologia 179, 1–14 (2015).

    ADS  PubMed  Article  PubMed Central  Google Scholar 

  • 24.

    Bakkali, F., Averbeck, S., Averbeck, D. & Idaomar, M. Biological effects of essential oils—A review. Food Chem. Toxicol. 46, 446–475 (2008).

    CAS  Article  Google Scholar 

  • 25.

    Mithöfer, A. & Boland, W. Plant defense against herbivores: Chemical aspects. Annu. Rev. Plant Biol. 63, 431–450 (2012).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 26.

    Douglas, A. Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera. Annu. Rev. Entomol. 43, 17–37 (1998).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 27.

    Ayres, M. P., Wilkens, R. T., Ruel, J. J., Lombardero, M. J. & Vallery, E. Nitrogen budgets of phloem-feeding bark beetles with and without symbiotic fungi. Ecology 81, 2198–2210 (2000).

    Article  Google Scholar 

  • 28.

    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. 39, 1133–1147 (2009).

    CAS  Article  Google Scholar 

  • 29.

    Cardoza, Y. J., Moser, J. C., Klepzig, K. D. & Raffa, K. F. Multipartite symbioses among fungi, mites, nematodes, and the spruce beetle, Dendroctonus rufipennis. Environ. Entomol. 37, 956–963 (2008).

    PubMed  Article  PubMed Central  Google Scholar 

  • 30.

    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 179, 467–485 (2015).

    ADS  PubMed  Article  PubMed Central  Google Scholar 

  • 31.

    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. 64, 268–278 (2012).

    PubMed  Article  PubMed Central  Google Scholar 

  • 32.

    Delalibera, I. Jr., Handelsman, J. & Raffa, K. F. 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. 34, 541–547 (2005).

    Article  Google Scholar 

  • 33.

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

    Article  Google Scholar 

  • 34.

    Menéndez, E. et al. Pseudomonas coleopterorum sp. nov., a cellulase-producing bacterium isolated from the bark beetle Hylesinus fraxini. Int. J. Syst. Evol. Microbiol. 65, 2852–2858 (2015).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 35.

    Boone, C. K. et al. Bacteria associated with a tree-killing insect reduce concentrations of plant defense compounds. J. Chem. Ecol. 39, 1003–1006 (2013).

    CAS  PubMed  Article  Google Scholar 

  • 36.

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 37.

    Berasategui, A. et al. Gut microbiota of the pine weevil degrades conifer diterpenes and increases insect fitness. Mol. Ecol. 26, 4099–4110 (2017).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 38.

    Engl, T. & Kaltenpoth, M. Influence of microbial symbionts on insect pheromones. Nat. Prod. Rep. 35, 386–397 (2018).

    CAS  PubMed  Article  Google Scholar 

  • 39.

    Howe, M., Keefover-Ring, K. & Raffa, K. F. Pine engravers carry bacterial communities whose members reduce concentrations of host monoterpenes with variable degrees of redundancy, specificity, and capability. Environ. Entomol. 47, 638–645 (2018).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 40.

    Xu, L., Lou, Q., Cheng, C., Lu, M. & Sun, J. Gut-associated bacteria of Dendroctonus valens and their involvement in verbenone production. Microb. Ecol. 70, 1012–1023 (2015).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 41.

    Skrodenytė-Arbačiauskienė, V., Radžiutė, S., Stunžėnas, V. & Būda, V. Erwiniatypographi sp. nov., isolated from bark beetle (Ips typographus) gut. Int. J. Syst. Evol. Microbiol. 62, 942–948 (2012).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 42.

    Smith, D. J., Park, J., Tiedje, J. M. & Mohn, W. W. A large gene cluster in Burkholderia xenovorans encoding abietane diterpenoid catabolism. J. Bacteriol. 189, 6195–6204 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 43.

    Martin, V. J. & Mohn, W. W. Genetic investigation of the catabolic pathway for degradation of abietane diterpenoids by Pseudomonas abietaniphila BKME-9. J. Bacteriol. 182, 3784–3793 (2000).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 44.

    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. 35, 9–20 (2011).

    Google Scholar 

  • 45.

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

    Google Scholar 

  • 46.

    Sevim, A., Gökçe, C., Erbaş, Z. & Özkan, F. Bacteria from Ips sexdentatus (Coleoptera: Curculionidae) and their biocontrol potential. J. Basic Microbiol. 52, 695–704 (2012).

    PubMed  Article  PubMed Central  Google Scholar 

  • 47.

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

    Google Scholar 

  • 48.

    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).

  • 49.

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

  • 50.

    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. 114, 77–85 (2017).

    Article  Google Scholar 

  • 51.

    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).

  • 52.

    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).

  • 53.

    Villari, C. et al. Nutritional and pathogenic fungi associated with the pine engraver beetle trigger comparable defenses in Scots pine. Tree Physiol. 32, 867–879 (2012).

    PubMed  Article  PubMed Central  Google Scholar 

  • 54.

    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. 33, 239–249 (2008).

    Article  Google Scholar 

  • 55.

    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. 399, 188–196 (2017).

    Article  Google Scholar 

  • 56.

    Engel, P. & Moran, N. A. The gut microbiota of insects–diversity in structure and function. FEMS Microbiol. Rev. 37, 699–735 (2013).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 57.

    Hernández-García, J. A., Briones-Roblero, C. I., Rivera-Orduña, F. N. & Zúñiga, G. Revealing the gut bacteriome of Dendroctonus bark beetles (Curculionidae: Scolytinae): Diversity, core members and co-evolutionary patterns. Sci. Rep. 7, 1–12 (2017).

    Article  CAS  Google Scholar 

  • 58.

    Morrison, M. & Miron, J. Adhesion to cellulose by Ruminococcus albus: A combination of cellulosomes and Pil-proteins?. FEMS Microbiol. Lett. 185, 109–115 (2000).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 59.

    Fabryová, A. et al. On the bright side of a forest pest-the metabolic potential of bark beetles’ bacterial associates. Sci. Total Environ. 619, 9–17 (2018).

    ADS  PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 60.

    Briones-Roblero, C. I. et al. Structure and dynamics of the gut bacterial microbiota of the bark beetle, Dendroctonus rhizophagus (Curculionidae: Scolytinae) across their life stages. PLoS ONE 12, e0175470 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 61.

    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. 7, 1–10 (2004).

    Google Scholar 

  • 62.

    Horne, I., Haritos, V. S. & Oakeshott, J. G. Comparative and functional genomics of lipases in holometabolous insects. Insect Biochem. Mol. Biol. 39, 547–567 (2009).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 63.

    Arrese, E. L. & Soulages, J. L. Insect fat body: Energy, metabolism, and regulation. Annu. Rev. Entomol. 55, 207–225 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 64.

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

    Article  Google Scholar 

  • 65.

    Morales-Jiménez, J. et al. Nitrogen-fixing and uricolytic bacteria associated with the gut of Dendroctonus rhizophagus and Dendroctonus valens (Curculionidae: Scolytinae). Microb. Ecol. 66, 200–210 (2013).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 66.

    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. 58, 879–891 (2009).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 67.

    Menna, P. M. & 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. 61, 3052–3067 (2011).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 68.

    Chen, W.-M. et al. Legume symbiotic nitrogen fixation byβ-proteobacteria is widespread in nature. J. Bacteriol. 185, 7266–7272 (2003).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 69.

    Gurevitch, J., Scheiner, S. M. & Fox, G. A. The Ecology of Plants (Sinauer Associates, Sunderland, 2002).

    Google Scholar 

  • 70.

    Gibson, C. M. & Hunter, M. S. Extraordinarily widespread and fantastically complex: Comparative biology of endosymbiotic bacterial and fungal mutualists of insects. Ecol. Lett. 13, 223–234 (2010).

    PubMed  Article  PubMed Central  Google Scholar 

  • 71.

    Six, D. L. & Bentz, B. J. Fungi associated with the North American spruce beetle, Dendroctonus rufipennis. Can. J. For. Res. 33, 1815–1820 (2003).

    Article  Google Scholar 

  • 72.

    Naik, P. R. & Sakthivel, N. Functional characterization of a novel hydrocarbonoclastic Pseudomonas sp. strain PUP6 with plant-growth-promoting traits and antifungal potential. Res. Microbiol. 157, 538–546 (2006).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 73.

    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. 22, 326–330 (2012).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 74.

    Elsden, S. R., Hilton, M. G. & Waller, J. M. The end products of the metabolism of aromatic amino acids by Clostridia. Arch. Microbiol. 107, 283–288 (1976).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 75.

    Byers, J. & Birgersson, G. Pheromone production in a bark beetle independent of myrcene precursor in host pine species. Naturwissenschaften 77, 385–387 (1990).

    ADS  CAS  Article  Google Scholar 

  • 76.

    Blomquist, G. J. et al. Pheromone production in bark beetles. Insect Biochem. Mol. Biol. 40, 699–712 (2010).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 77.

    Cao, Q. et al. Effect of oxygen on verbenone conversion from cis-verbenol by gut facultative anaerobes of Dendroctonus valens. Front. Microbiol. 9, 464 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • 78.

    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. 108, 941–949 (2015).

    CAS  Article  Google Scholar 

  • 79.

    Durand, A.-A. et al. Surveying the endomicrobiome and ectomicrobiome of bark beetles: The case of Dendroctonus simplex. Sci. Rep. 5, 17190 (2015).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 80.

    Scott, J. J. et al. Bacterial protection of beetle-fungus mutualism. Science 322, 63–63 (2008).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 81.

    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. 49, 267–275 (1999).

    CAS  Article  Google Scholar 

  • 82.

    Santos-Garcia, D., Silva, F. J., Morin, S., Dettner, K. & Kuechler, S. M. 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. 9, 2893–2910 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 83.

    Lawson, E. T., Mousseau, T. A., Klaper, R., Hunter, M. D. & Werren, J. H. Rickettsia associated with male-killing in a buprestid beetle. Heredity 86, 497–505 (2001).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 84.

    Hurst, G. & Jiggins, F. M. Male-killing bacteria in insects: Mechanisms, incidence, and implications. Emerg. Infect. Dis. 6, 329 (2000).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 85.

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

  • 86.

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

  • 87.

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

  • 88.

    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).

  • 89.

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

    Google Scholar 

  • 90.

    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. 41, e1–e1 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 91.

    Magoč, T. & Salzberg, S. L. FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963 (2011).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 92.

    Bokulich, N. A. et al. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat. Methods 10, 57–59 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 93.

    Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 94.

    Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 95.

    Edgar, R. C. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996 (2013).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 96.

    Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 97.

    Quast, C. et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2012).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 98.

    Edgar, R. C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 99.

    Chao, A., Lee, S.-M. & Chen, T.-C. A generalized Good’s nonparametric coverage estimator. Chin. J. Math. 16, 189–199 (1988).

    MathSciNet  MATH  Google Scholar 

  • 100.

    Magurran, A. E. Ecological Diversity and its Measurement (Princeton University Press, Princeton, 1988).

    Google Scholar 

  • 101.

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

  • 102.

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

  • 103.

    Lozupone, C. A., Hamady, M., Kelley, S. T. & Knight, R. Quantitative and qualitative β diversity measures lead to different insights into factors that structure microbial communities. Appl. Environ. Microbiol. 73, 1576–1585 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 104.

    Clarke, K. R. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18, 117–143 (1993).

    Article  Google Scholar 

  • 105.

    Cai, L. Multi-response permutation procedure as an alternative to the analysis of variance: An SPSS implementation. Behav. Res. Methods 38, 51–59 (2006).

    PubMed  Article  Google Scholar 

  • 106.

    Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral. Ecol. 26, 32–46 (2001).

    Google Scholar 

  • 107.

    Excoffier, L., Smouse, P. E. & Quattro, J. M. Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131, 479–491 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 108.

    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. 325340, 1–10 (2014).

    Article  CAS  Google Scholar 

  • 109.

    Paulson, J. N., Pop, M. & Bravo, H. C. Metastats: An improved statistical method for analysis of metagenomic data. Genome Biol. 12, P17 (2011).

    PubMed Central  Article  PubMed  Google Scholar 

  • 110.

    Segata, N. et al. Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60 (2011).

    PubMed  PubMed Central  Article  Google Scholar 

  • 111.

    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).

  • 112.

    Kanehisa, M., Goto, S., Sato, Y., Furumichi, M. & Tanabe, M. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 40, D109–D114 (2012).

    CAS  PubMed  Article  PubMed Central  Google Scholar 


  • Source: Ecology - nature.com

    Dietary diversity and evolution of the earliest flying vertebrates revealed by dental microwear texture analysis

    Saudi Arabia faces increased heat, humidity, precipitation extremes by mid-century