{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,9]],"date-time":"2026-10-09T18:47:50Z","timestamp":1791571670837,"version":"4.3.4"},"reference-count":86,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,7,7]],"date-time":"2023-07-07T00:00:00Z","timestamp":1688688000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>\n                    The close association between bacteria and insect hosts has played an indispensable role in insect diversity and ecology. Thus, continued characterization of such insect-associated-microbial communities is imperative, especially those of saprophagous scarab beetles. The bacterial community of the digestive tract of adults and larvae of the cetoniine scarab species\n                    <jats:italic>Cotinis nitida<\/jats:italic>\n                    is characterized according to life stage, gut structure, and sex via high-throughput 16S rRNA gene amplicon sequencing. Through permutational ANOVAs of the resulting sequences, bacterial communities of the digestive system are shown to differ significantly between adults and larvae in taxon richness, evenness and relatedness. Significant bacterial community-level differences are also observed between the midgut and hindgut in adult beetles, while no significant host-sex differences are observed. The partitioning between bacterial communities in the larval digestive system is shown through significant differences in two distinct hindgut regions, the ileum and the expanded paunch, but not between the midgut and ileum portion of the hindgut region. These data further corroborate the hypothesis of strong community partitioning in the gut of members of the Scarabaeoidea, suggest hypotheses of physiological-digestive association, and also demonstrate the presence of a seemingly unusual non-scarab-associated taxon. These findings contribute to a general portrait of scarabaeoid digestive tract bacterial communities while illuminating the microbiome of a common new world cetoniine of the Gymnetini\u2014a tribe largely neglected in scarab and beetle microbiome and symbiosis literature.\n                  <\/jats:p>","DOI":"10.3389\/fmicb.2023.1185661","type":"journal-article","created":{"date-parts":[[2023,7,7]],"date-time":"2023-07-07T12:33:58Z","timestamp":1688733238000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":15,"title":["Gut bacteria of adult and larval Cotinis nitida Linnaeus (Coleoptera: Scarabaeidae) demonstrate community differences according to respective life stage and gut region"],"prefix":"10.3389","volume":"14","author":[{"given":"Roy A.","family":"Kucuk","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Barbara J.","family":"Campbell","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicholas J.","family":"Lyon","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emily A.","family":"Shelby","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael S.","family":"Caterino","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,7,7]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"1055","DOI":"10.1053\/j.gastro.2014.07.020","article-title":"Correlation between intraluminal oxygen gradient and radial partitioning of intestinal microbiota","volume":"147","author":"Albenberg","year":"2014","journal-title":"Gastroenterology"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"291","DOI":"10.3389\/fmicb.2017.00291","article-title":"Bacterial community and PHB-accumulating Bacteria associated with the wall and specialized niches of the hindgut of the Forest cockchafer (Melolontha hippocastani)","volume":"8","author":"Alonso-Pernas","year":"","journal-title":"Front. Microbiol."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"1970","DOI":"10.3389\/fmicb.2017.01970","article-title":"In vivo isotopic labeling of symbiotic Bacteria involved in cellulose degradation and nitrogen recycling within the gut of the Forest cockchafer (Melolontha hippocastani)","volume":"8","author":"Alonso-Pernas","year":"","journal-title":"Front. Microbiol."},{"key":"ref007","doi-asserted-by":"crossref","first-page":"e00191","DOI":"10.1128\/mSystems.00191-16","article-title":"Deblur Rapidly Resolves Single-Nucleotide Community Sequence Patterns","volume":"2","author":"Amir","year":"2017","journal-title":"mSystems"},{"key":"ref4","doi-asserted-by":"crossref","DOI":"10.1002\/9781118445112.stat07841","article-title":"Permutational multivariate analysis of variance (PERMANOVA)","volume-title":"Wiley StatsRef: statistics reference online","author":"Anderson","year":"2017"},{"key":"ref003","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1111\/j.1574-6941.2010.00950.x","article-title":"Inter- and intraspecific comparison of the bacterial assemblages in the hindgut of humivorous scarab beetle larvae (Pachnoda spp.)","volume":"74","author":"Andert","year":"2010","journal-title":"FEMS Microbiol Ecol."},{"key":"ref5","doi-asserted-by":"publisher","first-page":"129","DOI":"10.3354\/ame01753","article-title":"Minor revision to v4 region rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton","volume":"75","author":"Apprill","year":"2015","journal-title":"Aquat. Microb. Ecol."},{"key":"ref004","doi-asserted-by":"crossref","first-page":"e51557","DOI":"10.1371\/journal.pone.0051557","article-title":"Comparative evaluation of the gut microbiota associated with the below- and above-ground life stages (larvae and beetles) of the forest cockchafer","volume":"7","author":"Arias-Cordero","year":"2012","journal-title":"Melolontha hippocastani. PLoS One."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"627","DOI":"10.3390\/d5030627","article-title":"Untangling the genetic basis of Fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in diverse gut communities","volume":"5","author":"Biddle","year":"2013","journal-title":"Diversity"},{"key":"ref009","first-page":"2","article-title":"qiime2R: Importing QIIME2 artifacts and associated data into R sessions","author":"Bisanz","year":"2018","journal-title":"Version"},{"key":"ref006","doi-asserted-by":"crossref","first-page":"1091","DOI":"10.1038\/s41587-019-0252-6","article-title":"Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2","volume":"37","author":"Bolyen","year":"2019","journal-title":"Nat Biotechnol.Nat Biotechnol"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"8406846","DOI":"10.1155\/2020\/8406846","article-title":"Alteration of intestinal microbiota in 3-deoxyglucosone-induced Prediabetic rats","volume":"2020","author":"Cai","year":"2020","journal-title":"Biomed. Res. Int."},{"key":"ref005","doi-asserted-by":"crossref","first-page":"e103","DOI":"10.1093\/nar\/gkz569","article-title":"High-throughput amplicon sequencing of the full-length 16S rRNA gene with single-nucleotide resolution","volume":"47","author":"Callahan","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref10","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1023\/A:1023325817663","article-title":"Promicromonospora pachnodae sp. nov., a member of the (hemi)cellulolytic hindgut flora of larvae of the scarab beetle Pachnoda marginata","volume":"83","author":"Cazemier","year":"2003","journal-title":"Antonie Van Leeuwenhoek"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"4099","DOI":"10.1128\/AEM.65.9.4099-4107.1999","article-title":"Molecular and biochemical characterization of two xylanase-encoding genes from Cellulomonas pachnodae","volume":"65","author":"Cazemier","year":"1999","journal-title":"Appl. Environ. Microbiol."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"1129","DOI":"10.1007\/s10295-015-1632-7","article-title":"Persistence of Methanosaeta populations in anaerobic digestion during process instability","volume":"42","author":"Chen","year":"2015","journal-title":"J. Ind. Microbiol. Biotechnol."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"123963","DOI":"10.1016\/j.biortech.2020.123963","article-title":"Effects of digestate recirculation ratios on biogas production and methane yield of continuous dry anaerobic digestion","volume":"316","author":"Chen","year":"2020","journal-title":"Bioresour. Technol."},{"key":"ref001","doi-asserted-by":"crossref","first-page":"516","DOI":"10.1038\/s41467-019-08438-0","article-title":"The antimicrobial potential of Streptomyces from insect microbiomes","volume":"10","author":"Chevrette","year":"2019","journal-title":"Nat. Commun."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"4343","DOI":"10.1111\/1462-2920.14797","article-title":"Developmental stages and gut microenvironments influence gut microbiota dynamics in the invasive beetle Popillia japonica Newman (Coleoptera: Scarabaeidae)","volume":"21","author":"Chouaia","year":"2019","journal-title":"Environ. Microbiol."},{"key":"ref15","volume-title":"RRPP: Linear model evaluation with randomized residuals in a permutation procedure","author":"Collyer","year":"2021"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"3566","DOI":"10.1890\/08-1823.1","article-title":"Associations between species and groups of sites: indices and statistical inference","volume":"90","author":"De C\u00e1ceres","year":"2009","journal-title":"Ecology"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"973","DOI":"10.1111\/j.2041-210X.2012.00246.x","article-title":"Using species combinations in indicator value analyses","volume":"3","author":"De C\u00e1ceres","year":"2012","journal-title":"Methods Ecol. Evol."},{"key":"ref18","doi-asserted-by":"publisher","first-page":"126050","DOI":"10.1016\/j.syapm.2019.126050","article-title":"Lacipirellula parvula gen. nov., sp. nov., representing a lineage of planctomycetes widespread in low-oxygen habitats, description of the family Lacipirellulaceae fam. nov. and proposal of the orders Pirellulales ord. nov., Gemmatales ord. nov. and Isosphaerales ord. nov","volume":"43","author":"Dedysh","year":"2020","journal-title":"Syst. Appl. Microbiol."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1038\/nrmicro3552","article-title":"Gut biogeography of the bacterial microbiota","volume":"14","author":"Donaldson","year":"2016","journal-title":"Nat. Rev. Microbiol."},{"key":"ref20","doi-asserted-by":"publisher","first-page":"e02100","DOI":"10.1128\/AEM.02100-20","article-title":"Hindgut microbiota reflects different digestive strategies in dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae)","volume":"87","author":"Ebert","year":"2021","journal-title":"Appl. Environ. Microbiol."},{"key":"ref21","doi-asserted-by":"publisher","first-page":"4556","DOI":"10.1128\/AEM.71.8.4556-4566.2005","article-title":"Structure and topology of microbial communities in the major gut compartments of Melolontha larvae (Coleoptera: Scarabaeidae)","volume":"71","author":"Egert","year":"2005","journal-title":"Appl. Environ. Microbiol."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"6659","DOI":"10.1128\/AEM.69.11.6659-6668.2003","article-title":"Microbial community structure in midgut and hindgut of the humus-feeding larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae)","volume":"69","author":"Egert","year":"2003","journal-title":"Appl. Environ. Microbiol."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"699","DOI":"10.1111\/1574-6976.12025","article-title":"The gut microbiota of insects \u2013 diversity in structure and function","volume":"37","author":"Engel","year":"2013","journal-title":"FEMS Microbiol. Rev."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s13568-017-0531-x","article-title":"Methanogens: biochemical background and biotechnological applications","volume":"8","author":"Enzmann","year":"2018","journal-title":"AMB Express"},{"key":"ref25","doi-asserted-by":"publisher","first-page":"e79061","DOI":"10.1371\/journal.pone.0079061","article-title":"Brood ball-mediated transmission of microbiome members in the dung beetle, Onthophagus taurus (Coleoptera: Scarabaeidae)","volume":"8","author":"Estes","year":"2013","journal-title":"PLoS One"},{"key":"ref26","doi-asserted-by":"publisher","first-page":"789","DOI":"10.1016\/j.cell.2014.09.053","article-title":"Human genetics shape the gut microbiome","volume":"159","author":"Goodrich","year":"2014","journal-title":"Cells"},{"key":"ref27","doi-asserted-by":"publisher","first-page":"20190068","DOI":"10.1098\/rstb.2019.0068","article-title":"Links between metamorphosis and symbiosis in holometabolous insects","volume":"374","author":"Hammer","year":"2019","journal-title":"Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"608","DOI":"10.1603\/0046-225x(2008)37[608:jbffbg]2.0.co;2","article-title":"Japanese beetles facilitate feeding by green June beetles (Coleoptera: Scarabaeidae) on ripening grapes","volume":"37","author":"Hammons","year":"2008","journal-title":"Environ. Entomol."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"e21370","DOI":"10.1002\/arch.21370","article-title":"Characterization of cellulose degrading bacteria from the larval gut of the white grub beetle Lepidiota mansueta (Coleoptera: Scarabaeidae)","volume":"94","author":"Handique","year":"2017","journal-title":"Arch. Insect Biochem. Physiol."},{"key":"ref30","author":"Hester","year":"2021"},{"key":"ref32","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1016\/j.syapm.2012.03.003","article-title":"Humic substance-mediated Fe(III) reduction by a fermenting Bacillus strain from the alkaline gut of a humus-feeding scarab beetle larva","volume":"35","author":"Hobbie","year":"2012","journal-title":"Syst. Appl. Microbiol."},{"key":"ref33","doi-asserted-by":"publisher","first-page":"2189","DOI":"10.1099\/00207713-50-6-2189","article-title":"Dysgonomonas gen. nov. to accommodate Dysgonomonas gadei sp. nov., an organism isolated from a human gall bladder, and Dysgonomonas capnocytophagoides (formerly CDC group DF-3)","author":"Hofstad","year":"2000","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref010","doi-asserted-by":"crossref","first-page":"e0238022","DOI":"10.1128\/spectrum.02380-22","article-title":"Novel Insights into the Pig Gut Microbiome Using Metagenome-Assembled Genomes","volume":"10","author":"Holman","year":"2022","journal-title":"Microbiol Spectr."},{"key":"ref34","doi-asserted-by":"publisher","first-page":"104408","DOI":"10.1016\/j.isci.2022.104408","article-title":"Microbiome assembly on Drosophila body surfaces benefits the flies to combat fungal infections","volume":"25","author":"Hong","year":"2022","journal-title":"iScience"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"e899","DOI":"10.1002\/mbo3.899","article-title":"Shared and unique microbes between small hive beetles (Aethina tumida) and their honey bee hosts","volume":"8","author":"Huang","year":"2019","journal-title":"Microbiology"},{"key":"ref38","doi-asserted-by":"publisher","first-page":"e57169","DOI":"10.1371\/journal.pone.0057169","article-title":"The impact of environmental heterogeneity and life stage on the hindgut microbiota of Holotrichia parallela larvae (Coleoptera: Scarabaeidae)","volume":"8","author":"Huang","year":"2013","journal-title":"PLoS One"},{"key":"ref40","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1186\/s40168-020-00823-y","article-title":"Most dominant roles of insect gut bacteria: digestion, detoxification, or essential nutrient provision?","volume":"8","author":"Jing","year":"2020","journal-title":"Microbiome"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1093\/ee\/20.1.15","article-title":"The role of Trichosporon cutaneum in eliciting aggregation behavior in Cotinis nitida. (Coleoptera: Scarabeidae)","volume":"20","author":"Johnson","year":"1991","journal-title":"Environ. Entomol."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"5014","DOI":"10.1111\/1462-2920.15435","article-title":"Shifting microbiomes complement life stage transitions and diet of the bird parasite Philornis downsi from the Galapagos Islands","volume":"23","author":"Jose","year":"2021","journal-title":"Environ. Microbiol."},{"key":"ref008","doi-asserted-by":"crossref","first-page":"3059","DOI":"10.1093\/nar\/gkf436","article-title":"MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform","volume":"30","author":"Katoh","year":"2002","journal-title":"Nucleic Acids Res."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"8618","DOI":"10.1073\/pnas.1200231109","article-title":"Symbiont-mediated insecticide resistance","volume":"109","author":"Kikuchi","year":"2012","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"5112","DOI":"10.1128\/AEM.01043-13","article-title":"Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform","volume":"79","author":"Kozich","year":"2013","journal-title":"Appl. Environ. Microbiol."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"11494","DOI":"10.1038\/s41598-021-90885-1","article-title":"The keystone commensal bacterium Christensenella minuta DSM 22607 displays anti-inflammatory properties both in vitro and in vivo","volume":"11","author":"Kropp","year":"2021","journal-title":"Sci. Rep."},{"key":"ref46","doi-asserted-by":"publisher","first-page":"005081","DOI":"10.1099\/ijsem.0.005081","article-title":"Zophobihabitans entericus gen. Nov., sp. nov., a new member of the family Orbaceae isolated from the gut of a superworm Zophobas morio","volume":"71","author":"Kuo","year":"2021","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1007\/s12275-018-8024-4","article-title":"The Ruminococci: key symbionts of the gut ecosystem","volume":"56","author":"La Reau","year":"2018","journal-title":"J. Microbiol."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"238","DOI":"10.1186\/s12866-019-1601-9","article-title":"Diet is not the primary driver of bacterial community structure in the gut of litter-feeding cockroaches","volume":"19","author":"Lampert","year":"2019","journal-title":"BMC Microbiol."},{"key":"ref49","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1038\/ismej.2010.133","article-title":"UNiFrac: an effective distance metric for microbial community comparison","volume":"5","author":"Lozupone","year":"2011","journal-title":"ISME J."},{"key":"ref50","author":"Lyon","year":"2021"},{"key":"ref51","author":"Lyon","year":"2023"},{"key":"ref52","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1186\/s40168-017-0397-9","article-title":"An IMD-like pathway mediates both endosymbiont control and host immunity in the cereal weevil Sitophilus spp","volume":"6","author":"Maire","year":"2018","journal-title":"Microbiome."},{"key":"ref54","doi-asserted-by":"publisher","first-page":"24729","DOI":"10.1073\/pnas.1909655116","article-title":"The evolution and genomic basis of beetle diversity","volume":"116","author":"McKenna","year":"2019","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"ref55","doi-asserted-by":"publisher","first-page":"2361","DOI":"10.3389\/fmicb.2018.02361","article-title":"Bacterial associates of a gregarious riparian beetle with explosive defensive chemistry","volume":"9","author":"McManus","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref56","doi-asserted-by":"publisher","first-page":"1256","DOI":"10.1128\/AEM.03700-15","article-title":"Deterministic assembly of complex bacterial communities in guts of germ-free cockroaches","volume":"82","author":"Mikaelyan","year":"2016","journal-title":"Appl. Environ. Microbiol."},{"key":"ref57","author":"Oksanen","year":"2020"},{"key":"ref58","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1093\/bioinformatics\/btg412","article-title":"APE: analyses of phylogenetics and evolution in R language","volume":"20","author":"Paradis","year":"2004","journal-title":"Bioinformatics"},{"key":"ref59","doi-asserted-by":"publisher","first-page":"906","DOI":"10.3389\/fimmu.2020.00906","article-title":"The genus Alistipes: gut Bacteria with emerging implications to inflammation, Cancer, and mental health","volume":"11","author":"Parker","year":"2020","journal-title":"Front. Immunol."},{"key":"ref60","doi-asserted-by":"publisher","first-page":"383","DOI":"10.1146\/annurev.en.36.010191.002123","article-title":"Ecology and management of turfgrass insects","volume":"36","author":"Potter","year":"1991","journal-title":"Annu. Rev. Entomol."},{"key":"ref61","doi-asserted-by":"publisher","first-page":"681","DOI":"10.1099\/ijs.0.070391-0","article-title":"Dysgonomonas termitidis sp. nov., isolated from the gut of the subterranean termite Reticulitermes speratus","volume":"65","author":"Pramono","year":"2015","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref62","doi-asserted-by":"publisher","first-page":"e9490","DOI":"10.1371\/journal.pone.0009490","article-title":"FastTree 2\u2013approximately maximum-likelihood trees for large alignments","volume":"5","author":"Price","year":"2010","journal-title":"PLoS One"},{"key":"ref002","first-page":"4","volume-title":"Microbiome innovation in agriculture: development of microbial based tools for insect pest management","author":"Qadri","year":"2020"},{"key":"ref63","doi-asserted-by":"publisher","first-page":"D590","DOI":"10.1093\/nar\/gks1219","article-title":"The SILVA ribosomal RNA gene database project: improved data processing and web-based tools","volume":"41","author":"Quast","year":"2013","journal-title":"Nucleic Acids Res."},{"key":"ref011","volume-title":"R: A language and environment for statistical computing","year":"2020"},{"key":"ref012","doi-asserted-by":"crossref","first-page":"13582","DOI":"10.1073\/pnas.1312524110","article-title":"Metabolic niche of a prominent sulfate-reducing human gut bacterium","volume":"110","author":"Rey","year":"2013","journal-title":"Proc. Natl. Acad. Sci. U S A."},{"key":"ref64","doi-asserted-by":"publisher","first-page":"164","DOI":"10.1186\/s12866-019-1540-5","article-title":"Taxonomic features and comparisons of the gut microbiome from two edible fungus-farming termites (Macrotermes falciger; M. natalensis) harvested in the Vhembe district of Limpopo, South Africa","volume":"19","author":"Schnorr","year":"2019","journal-title":"BMC Microbiol."},{"key":"ref65","doi-asserted-by":"publisher","first-page":"761","DOI":"10.3390\/microorganisms10040761","article-title":"Enrichment of anaerobic microbial communities from Midgut and hindgut of Sun beetle larvae (Pachnoda marginata) on wheat straw: effect of inoculum preparation","volume":"10","author":"Schroeder","year":"2022","journal-title":"Microorganisms."},{"key":"ref66","doi-asserted-by":"publisher","first-page":"679","DOI":"10.1086\/688926","article-title":"Developmental and ecological benefits of the maternally transmitted microbiota in a dung beetle","volume":"188","author":"Schwab","year":"2016","journal-title":"Am. Nat."},{"key":"ref67","doi-asserted-by":"publisher","first-page":"6092","DOI":"10.1111\/mec.13901","article-title":"Gut microbiota of dung beetles correspond to dietary specializations of adults and larvae","volume":"25","author":"Shukla","year":"2016","journal-title":"Mol. Ecol."},{"key":"ref69","doi-asserted-by":"publisher","first-page":"1698","DOI":"10.3389\/fmicb.2020.01698","article-title":"Diversity and composition of the gut microbiota in the developmental stages of the dung beetle Copris incertus say (Coleoptera, Scarabaeidae)","volume":"11","author":"Su\u00e1rez-Moo","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref013","article-title":"Git \u2013 fast, scalable, distributed revision control system","author":"Torvalds","year":"2021"},{"key":"ref70","first-page":"16","article-title":"Fossil: Palaeoecological and Palaeogeographical analysis tools","volume-title":"Palaeontologia Electronica","author":"Vavrek","year":"2020"},{"key":"ref71","doi-asserted-by":"publisher","first-page":"471","DOI":"10.1080\/00275514.1990.12025910","article-title":"Development of a yeast Flora in the adult green June beetle (Cotinis nitida)","volume":"82","author":"Vishniac","year":"1990","journal-title":"Mycologia"},{"key":"ref72","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1186\/s40168-022-01291-2","article-title":"Lignocellulose degradation in Protaetia brevitarsis larvae digestive tract: refining on a tightly designed microbial fermentation production line","volume":"10","author":"Wang","year":"2022","journal-title":"Microbiome."},{"key":"ref73","doi-asserted-by":"crossref","first-page":"e03250","DOI":"10.1128\/AEM.03250-16","article-title":"Gut microbiota colonization and transmission in the burying beetle Nicrophorus vespilloides throughout development","volume":"83","author":"Wang","year":"2017","journal-title":"Appl. Environ. Microbiol."},{"key":"ref74","doi-asserted-by":"publisher","first-page":"719","DOI":"10.3390\/insects11100719","article-title":"Divergence in gut bacterial community among life stages of the rainbow stag beetle Phalacrognathus muelleri (Coleoptera: Lucanidae)","volume":"11","author":"Wang","year":"2020","journal-title":"Insects."},{"key":"ref75","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1099\/00207713-43-2-261","article-title":"Spiroplasma clarkii sp. nov. from the Green June Beetle (Coleoptera: Scarabaeidae)","volume":"43","author":"Whitcomb","year":"1993","journal-title":"Int. J. Syst. Bacteriol."},{"key":"ref76","article-title":"ggplot2: elegant graphics for data analysis","author":"Wickham","year":"2016"},{"key":"ref77","article-title":"Stringr: simple, Consistent Wrappers for Common String Operations","author":"Wickham","year":"2019"},{"key":"ref78","article-title":"Tidyverse: Easily Install and Load the \u201cTidyverse.\u201d","author":"Wickham","year":"2021"},{"key":"ref79","doi-asserted-by":"publisher","first-page":"e00186-20","DOI":"10.1128\/mSphere.00186-20","article-title":"Globally abundant \"Candidatus Udaeobacter\" benefits from release of antibiotics in soil and potentially performs trace gas scavenging","volume":"5","author":"Willms","year":"2020","journal-title":"mSphere"},{"key":"ref81","doi-asserted-by":"publisher","first-page":"399","DOI":"10.1038\/hdy.2013.118","article-title":"Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps","volume":"112","author":"Xie","year":"2014","journal-title":"Heredity (Edinb)."},{"key":"ref82","doi-asserted-by":"publisher","first-page":"e01326","DOI":"10.1128\/mBio.01326-16","article-title":"Metabolism of toxic sugars by strains of the bee gut Symbiont Gilliamella apicola","volume":"7","author":"Zheng","year":"2016","journal-title":"MBio"}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2023.1185661\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,7,7]],"date-time":"2023-07-07T12:34:19Z","timestamp":1688733259000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2023.1185661\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,7,7]]},"references-count":86,"alternative-id":["10.3389\/fmicb.2023.1185661"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2023.1185661","relation":{},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,7,7]]},"article-number":"1185661"}}