{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,24]],"date-time":"2026-01-24T10:59:50Z","timestamp":1769252390775,"version":"3.49.0"},"reference-count":82,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2023,7,31]],"date-time":"2023-07-31T00:00:00Z","timestamp":1690761600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"International Research Project-Integrated Pest Management of the invasive Japanese Beetle","award":["H2020-EU.3.2.1.1.\/ID: 861852"],"award-info":[{"award-number":["H2020-EU.3.2.1.1.\/ID: 861852"]}]},{"name":"IPM-Popillia project","award":["H2020-EU.3.2.1.1.\/ID: 861852"],"award-info":[{"award-number":["H2020-EU.3.2.1.1.\/ID: 861852"]}]},{"name":"M. Universidades\u2014Margarita Salas","award":["H2020-EU.3.2.1.1.\/ID: 861852"],"award-info":[{"award-number":["H2020-EU.3.2.1.1.\/ID: 861852"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Popillia japonica (Coleoptera: Scarabaeidae), is an emerging invasive pest in Europe and America. In the Azores, this pest was first found on Terceira Island during the sixties and soon spread to other islands. The rate of infestation differs between islands, and we hypothesized that microbiome composition could play a role. Therefore, we sampled 3rd instar larvae and soil from sites with high and low infestation rates to analyze the microbiome using next-generation sequencing. We analyzed twenty-four 16S DNA libraries, which resulted in 3278 operational taxonomic units. The alpha and beta diversity of the soil microbiome was similar between sites. In contrast, the larvae from high-density sites presented a higher bacterial gut diversity than larvae from low-density sites, with biomarkers linked to plant digestion, nutrient acquisition, and detoxification. Consequently, larvae from high-density sites displayed several enriched molecular functions associated with the families Ruminococcaceae, Clostridiaceae and Rikenellaceae. These bacteria revealed a supportive function by producing several CAZyme families and other proteins. These findings suggest that the microbiome must be one drive for the increase in P. japonica populations, thus providing a checkpoint in the establishment and spread of this pest.<\/jats:p>","DOI":"10.3390\/microorganisms11081972","type":"journal-article","created":{"date-parts":[[2023,8,1]],"date-time":"2023-08-01T09:14:40Z","timestamp":1690881280000},"page":"1972","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Exploring Gut Microbiome Variations between Popillia japonica Populations of Azores"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1373-6060","authenticated-orcid":false,"given":"Jorge","family":"Frias","sequence":"first","affiliation":[{"name":"Centro de Biotecnologia dos A\u00e7ores, Faculdade de Ci\u00eancias e Tecnologia, Universidade dos A\u00e7ores, 9500-321 Ponta Delgada, Portugal"}]},{"given":"Anna","family":"Garriga","sequence":"additional","affiliation":[{"name":"Centro de Biotecnologia dos A\u00e7ores, Faculdade de Ci\u00eancias e Tecnologia, Universidade dos A\u00e7ores, 9500-321 Ponta Delgada, Portugal"},{"name":"Departament de Biologia Animal, Vegetal i Ecologia, Facultat de Bioci\u00e8ncies, Universitat Aut\u00f2noma de Barcelona, 08193 Bellaterra, Spain"}]},{"given":"\u00c1ngel","family":"Pe\u00f1alver","sequence":"additional","affiliation":[{"name":"Centro de Biotecnologia dos A\u00e7ores, Faculdade de Ci\u00eancias e Tecnologia, Universidade dos A\u00e7ores, 9500-321 Ponta Delgada, Portugal"}]},{"given":"M\u00e1rio","family":"Teixeira","sequence":"additional","affiliation":[{"name":"Centro de Biotecnologia dos A\u00e7ores, Faculdade de Ci\u00eancias e Tecnologia, Universidade dos A\u00e7ores, 9500-321 Ponta Delgada, Portugal"}]},{"given":"Rub\u00e9n","family":"Beltr\u00ed","sequence":"additional","affiliation":[{"name":"Centro de Biotecnologia dos A\u00e7ores, Faculdade de Ci\u00eancias e Tecnologia, Universidade dos A\u00e7ores, 9500-321 Ponta Delgada, Portugal"}]},{"given":"Duarte","family":"Toubarro","sequence":"additional","affiliation":[{"name":"Centro de Biotecnologia dos A\u00e7ores, Faculdade de Ci\u00eancias e Tecnologia, Universidade dos A\u00e7ores, 9500-321 Ponta Delgada, Portugal"}]},{"given":"Nelson","family":"Sim\u00f5es","sequence":"additional","affiliation":[{"name":"Centro de Biotecnologia dos A\u00e7ores, Faculdade de Ci\u00eancias e Tecnologia, Universidade dos A\u00e7ores, 9500-321 Ponta Delgada, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2023,7,31]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1093\/jipm\/pmab043","article-title":"Japanese Beetle (Coleoptera: Scarabaeidae) Invasion of North America: History, Ecology, and Management","volume":"13","author":"Althoff","year":"2022","journal-title":"J. Integr. Pest Manag."},{"key":"ref_2","unstructured":"Sim\u00f5es, N., and Martins, A. (1985). Life Cycle of Popillia Japonica Newman (Coleoptera\u2014Scarabaeidae) in Terceira Island\u2014Azores, University of the Azores."},{"key":"ref_3","first-page":"99","article-title":"Suppression of the Japanese Beetle in the Azores: An Ecological Approach","volume":"39","author":"Martins","year":"1988","journal-title":"Ecol. Bull."},{"key":"ref_4","first-page":"101","article-title":"Japanese Beetle: Monitoring in the Azores with Semiochemicals","volume":"39","author":"Martins","year":"1988","journal-title":"Ecol. Bull."},{"key":"ref_5","first-page":"480","article-title":"Effectiveness of Steinernema Spp. and Heterorhabditis Bacteriophora against Popillia Japonica in the Azores","volume":"25","author":"Laumond","year":"1993","journal-title":"J. Nematol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1007\/BF02373084","article-title":"Factors Influencing Parasitism of Adult Japanese Beetles, Polillia Japonica (Col.: Scarabaeidae) by Entomopathogenic Nematodes","volume":"38","author":"Lacey","year":"1993","journal-title":"Entomophaga"},{"key":"ref_7","unstructured":"Simoes, N., and Rosa, J. (1994). Bulletin OILB SROP, OILB."},{"key":"ref_8","first-page":"215","article-title":"Natural Occurrence of Entomopathogenic Nematodes (Rhabditida: Steinernema, Heterorhabditis) in the Azores","volume":"32","author":"Rosa","year":"2000","journal-title":"J. Nematol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"439","DOI":"10.14411\/eje.2001.064","article-title":"Comparative Dispersal and Larvicidal Activity of Exotic and Azorean Isolates of Entomopathogenic Nematodes against Popillia Japonica (Coleoptera: Scarabaeidae)","volume":"98","author":"Lacey","year":"2001","journal-title":"Eur. J. Entomol."},{"key":"ref_10","unstructured":"Mendes, C., Lacey, L., Amaral, J., and Klien, M. (1994). Bulletin OILB SROP, OILB."},{"key":"ref_11","unstructured":"Popillia Japonica (POPIJA) [Portugal (Azores)] (2023, March 15). EPPO Global Database. Available online: https:\/\/gd.eppo.int\/taxon\/POPIJA\/distribution\/PT_az."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1093\/jee\/15.4.305","article-title":"Larval Food Habits of the Japanese Beetle (Popillia Japonica Newm.)","volume":"15","author":"Smith","year":"1922","journal-title":"J. Econ. Entomol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1038\/nrmicro.2017.87","article-title":"Embracing the Unknown: Disentangling the Complexities of the Soil Microbiome","volume":"15","author":"Fierer","year":"2017","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1016\/j.mib.2018.01.013","article-title":"The Soil Microbiome\u2014From Metagenomics to Metaphenomics","volume":"43","author":"Jansson","year":"2018","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"770","DOI":"10.1016\/j.tplants.2017.07.002","article-title":"Steering Soil Microbiomes to Suppress Aboveground Insect Pests","volume":"22","author":"Pineda","year":"2017","journal-title":"Trends Plant Sci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2199","DOI":"10.1128\/AEM.66.5.2199-2207.2000","article-title":"Localization of Symbiotic Clostridia in the Mixed Segment of the Termite Nasutitermes Takasagoensis (Shiraki)","volume":"66","author":"Tokuda","year":"2000","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"4170","DOI":"10.1111\/1462-2920.14420","article-title":"Metagenomic Analyses Highlight the Symbiotic Association between the Glacier Stonefly Andiperla Willinki and Its Bacterial Gut Community","volume":"20","author":"Murakami","year":"2018","journal-title":"Environ. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"340","DOI":"10.1111\/1744-7917.12143","article-title":"Metamicrobiomics in Herbivore Beetles of the Genus Cryptocephalus (Chrysomelidae): Toward the Understanding of Ecological Determinants in Insect Symbiosis","volume":"22","author":"Montagna","year":"2015","journal-title":"Insect Sci."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Li, D.-D., Li, J.-Y., Hu, Z.-Q., Liu, T.-X., and Zhang, S.-Z. (2022). Fall Armyworm Gut Bacterial Diversity Associated with Different Developmental Stages, Environmental Habitats, and Diets. Insects, 13.","DOI":"10.3390\/insects13090762"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Schroeder, B.G., Logro\u00f1o, W., da Rocha, U.N., Harms, H., and Nikolausz, M. (2022). Enrichment of Anaerobic Microbial Communities from Midgut and Hindgut of Sun Beetle Larvae (Pachnoda Marginata) on Wheat Straw: Effect of Inoculum Preparation. Microorganisms, 10.","DOI":"10.3390\/microorganisms10040761"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1603\/0046-225X-35.3.625","article-title":"Bacteria Associated with the Guts of Two Wood-Boring Beetles: Anoplophora Glabripennis and Saperda Vestita (Cerambycidae)","volume":"35","author":"Schloss","year":"2006","journal-title":"Environ. Entomol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"854513","DOI":"10.3389\/fmicb.2022.854513","article-title":"Soil Environments Influence Gut Prokaryotic Communities in the Larvae of the Invasive Japanese Beetle Popillia Japonica Newman","volume":"13","author":"Scharf","year":"2022","journal-title":"Front. Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Huang, S., and Zhang, H. (2013). The Impact of Environmental Heterogeneity and Life Stage on the Hindgut Microbiota of Holotrichia Parallela Larvae (Coleoptera: Scarabaeidae). PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0057169"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1111\/eea.12609","article-title":"Review of the Role of Gut Microbiota in Mass Rearing of the Olive Fruit Fly, Bactrocera Oleae, and Its Parasitoids","volume":"164","author":"Ras","year":"2017","journal-title":"Entomol. Exp. Appl."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1111\/eea.12768","article-title":"The Microbiome of Pest Insects: It Is Not Just Bacteria","volume":"167","author":"Gurung","year":"2019","journal-title":"Entomol. Exp. Appl."},{"key":"ref_26","unstructured":"(2023, February 28). Secretaria Regional da Agricultura e do Desenvolvimento Rural\u2014Secretaria Regional da Agricultura e do Desenvolvimento Rural\u2014Portal, Available online: https:\/\/portal.azores.gov.pt\/web\/sradr."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Melo, C.D., Maduro Dias, C.S.A.M., Wallon, S., Borba, A.E.S., Madruga, J., Borges, P.A.V., Ferreira, M.T., and Elias, R.B. (2022). Influence of Climate Variability and Soil Fertility on the Forage Quality and Productivity in Azorean Pastures. Agriculture, 12.","DOI":"10.3390\/agriculture12030358"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1097\/00010694-192705000-00002","article-title":"The Hydrometer as a New Method for the Mechanical Analysis of Soils","volume":"23","author":"Bouyoucos","year":"1927","journal-title":"Soil Sci."},{"key":"ref_29","unstructured":"Andrews, S., and Bittencourt, S. (2010). FastQC: A Quality Control Tool for High Throughput Sequence Data, Babraham Bioinformatics."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"10","DOI":"10.14806\/ej.17.1.200","article-title":"Cutadapt Removes Adapter Sequences from High-Throughput Sequencing Reads","volume":"17","author":"Martin","year":"2011","journal-title":"EMBnet J."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"852","DOI":"10.1038\/s41587-019-0209-9","article-title":"Reproducible, Interactive, Scalable and Extensible Microbiome Data Science Using QIIME 2","volume":"37","author":"Bolyen","year":"2019","journal-title":"Nat. Biotechnol."},{"key":"ref_32","doi-asserted-by":"crossref","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":"ref_33","unstructured":"Core Team, R. (2022). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"McMurdie, P.J., and Holmes, S. (2013). Phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0061217"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Andersen, K.S., Kirkegaard, R.H., Karst, S.M., and Albertsen, M. (2018). Ampvis2: An R Package to Analyse and Visualise 16S RRNA Amplicon Data. BioRxiv, preprint.","DOI":"10.1101\/299537"},{"key":"ref_36","unstructured":"Oksanen, F., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P., O\u2019Hara, R., Simpson, G., and Solymos, P. (2017). Vegan: Community Ecology Package, R Foundation for Statistical Computing. R Package Version 2.4\u20134."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"R60","DOI":"10.1186\/gb-2011-12-6-r60","article-title":"Metagenomic Biomarker Discovery and Explanation","volume":"12","author":"Segata","year":"2011","journal-title":"Genome Biol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1007\/s004420100716","article-title":"Ecologically Meaningful Transformations for Ordination of Species Data","volume":"129","author":"Legendre","year":"2001","journal-title":"Oecologia"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: A Flexible Trimmer for Illumina Sequence Data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Schmieder, R., and Edwards, R. (2011). Fast Identification and Removal of Sequence Contamination from Genomic and Metagenomic Datasets. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0017288"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1674","DOI":"10.1093\/bioinformatics\/btv033","article-title":"MEGAHIT: An Ultra-Fast Single-Node Solution for Large and Complex Metagenomics Assembly via Succinct de Bruijn Graph","volume":"31","author":"Li","year":"2015","journal-title":"Bioinformatics"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Hyatt, D., Chen, G.-L., LoCascio, P.F., Land, M.L., Larimer, F.W., and Hauser, L.J. (2010). Prodigal: Prokaryotic Gene Recognition and Translation Initiation Site Identification. BMC Bioinform., 11.","DOI":"10.1186\/1471-2105-11-119"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"5825","DOI":"10.1093\/molbev\/msab293","article-title":"EggNOG-Mapper v2: Functional Annotation, Orthology Assignments, and Domain Prediction at the Metagenomic Scale","volume":"38","author":"Cantalapiedra","year":"2021","journal-title":"Mol. Biol. Evol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1686","DOI":"10.21105\/joss.01686","article-title":"Welcome to the Tidyverse","volume":"4","author":"Wickham","year":"2019","journal-title":"J. Open Source Softw."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1639","DOI":"10.1101\/gr.092759.109","article-title":"Circos: An Information Aesthetic for Comparative Genomics","volume":"19","author":"Krzywinski","year":"2009","journal-title":"Genome Res."},{"key":"ref_46","doi-asserted-by":"crossref","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":"ref_47","doi-asserted-by":"crossref","first-page":"e01037-18","DOI":"10.1128\/AEM.01037-18","article-title":"Overlapping Community Compositions of Gut and Fecal Microbiomes in Lab-Reared and Field-Collected German Cockroaches","volume":"84","author":"Kakumanu","year":"2018","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/femsec\/fiu028","article-title":"Physicochemical Conditions, Metabolites and Community Structure of the Bacterial Microbiota in the Gut of Wood-Feeding Cockroaches (Blaberidae: Panesthiinae)","volume":"91","author":"Bauer","year":"2015","journal-title":"FEMS Microbiol. Ecol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1277","DOI":"10.1111\/j.1365-2672.2008.03867.x","article-title":"Autochthonous Bacterial Flora Indicated by PCR-DGGE of 16S RRNA Gene Fragments from the Alimentary Tract of Costelytra Zealandica (Coleoptera: Scarabaeidae)","volume":"105","author":"Zhang","year":"2008","journal-title":"J. Appl. Microbiol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"201","DOI":"10.3389\/fvets.2019.00201","article-title":"Development of the Caecal Microbiota in Three Broiler Breeds","volume":"6","author":"Richards","year":"2019","journal-title":"Front. Vet. Sci."},{"key":"ref_51","first-page":"311","article-title":"Xylan and Cellulose Utilization by the Clostridia","volume":"25","author":"Hazlewood","year":"1993","journal-title":"Biotechnol. Read. Mass"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1016\/0923-2508(92)90016-H","article-title":"Carbohydrate Assimilation by Saccharolytic Clostridia","volume":"143","author":"Mitchell","year":"1992","journal-title":"Res. Microbiol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1111\/j.1574-6968.1993.tb06501.x","article-title":"16S RDNA Analysis Reveals Phylogenetic Diversity among the Polysaccharolytic Clostridia","volume":"113","author":"Rainey","year":"1993","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"e02100-20","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":"ref_55","doi-asserted-by":"crossref","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 Melolontha Larvae (Coleoptera: Scarabaeidae)","volume":"71","author":"Egert","year":"2005","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"57","DOI":"10.2323\/jgam.51.57","article-title":"In Vitro and in Vivo Sulfate Reduction in the Gut Contents of the Termite Mastotermes Darwiniensis and the Rose-Chafer Pachnoda Marginata","volume":"51","author":"Limper","year":"2005","journal-title":"J. Gen. Appl. Microbiol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/S0723-2020(96)80039-7","article-title":"A Feasible Role of Sulfate-Reducing Bacteria in the Termite Gut","volume":"19","author":"Kuhnigk","year":"1996","journal-title":"Syst. Appl. Microbiol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"2758","DOI":"10.1128\/AEM.07788-11","article-title":"The Bacterial Community in the Gut of the Cockroach Shelfordella Lateralis Reflects the Close Evolutionary Relatedness of Cockroaches and Termites","volume":"78","author":"Schauer","year":"2012","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Arias-Cordero, E., Ping, L., Reichwald, K., Delb, H., Platzer, M., and Boland, W. (2012). Comparative Evaluation of the Gut Microbiota Associated with the Below- and Above-Ground Life Stages (Larvae and Beetles) of the Forest Cockchafer, Melolontha Hippocastani. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0051557"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"2222","DOI":"10.3389\/fmicb.2018.02222","article-title":"Screening of Phytophagous and Xylophagous Insects Guts Microbiota Abilities to Degrade Lignocellulose in Bioreactor","volume":"9","author":"Gales","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1111\/j.1574-6976.1995.tb00210.x","article-title":"Alcohol Dehydrogenase: Multiplicity and Relatedness in the Solvent-Producing Clostridia","volume":"17","author":"Chen","year":"1995","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/0005-2736(85)90339-6","article-title":"Phospholipid Aliphatic Chain Composition Modulates Lipid Class Composition, but Not Lipid Asymmetry in Clostridium Butyricum","volume":"813","author":"Johnston","year":"1985","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1128\/mr.50.4.484-524.1986","article-title":"Acetone-Butanol Fermentation Revisited","volume":"50","author":"Jones","year":"1986","journal-title":"Microbiol. Rev."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1007\/BF00446812","article-title":"Amino Acid Utilization Patterns in Clostridial Taxonomy","volume":"123","author":"Elsden","year":"1979","journal-title":"Arch. Microbiol."},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., and Thompson, F. (2014). The Prokaryotes: Alphaproteobacteria and Betaproteobacteria, Springer.","DOI":"10.1007\/978-3-642-30197-1"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"e10240","DOI":"10.7717\/peerj.10240","article-title":"Description of the Microbiota in Epidermal Mucus and Skin of Sharks (Ginglymostoma Cirratum and Negaprion Brevirostris) and One Stingray (Hypanus Americanus)","volume":"8","author":"Caballero","year":"2020","journal-title":"PeerJ"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"2930","DOI":"10.3390\/nu7042930","article-title":"The Role of Microbial Amino Acid Metabolism in Host Metabolism","volume":"7","author":"Neis","year":"2015","journal-title":"Nutrients"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"e2000426","DOI":"10.1002\/mnfr.202000426","article-title":"Functional Roles of B-Vitamins in the Gut and Gut Microbiome","volume":"64","author":"Uebanso","year":"2020","journal-title":"Mol. Nutr. Food Res."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"48","DOI":"10.3389\/fnut.2019.00048","article-title":"Metabolism of Dietary and Microbial Vitamin B Family in the Regulation of Host Immunity","volume":"6","author":"Yoshii","year":"2019","journal-title":"Front. Nutr."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1201","DOI":"10.3389\/fmicb.2015.01201","article-title":"Wolbachia and the Insect Immune System: What Reactive Oxygen Species Can Tell Us about the Mechanisms of Wolbachia\u2013Host Interactions","volume":"6","author":"Zug","year":"2015","journal-title":"Front. Microbiol."},{"key":"ref_71","doi-asserted-by":"crossref","unstructured":"Hirakawa, H., Kurushima, J., Hashimoto, Y., and Tomita, H. (2020). Progress Overview of Bacterial Two-Component Regulatory Systems as Potential Targets for Antimicrobial Chemotherapy. Antibiotics, 9.","DOI":"10.3390\/antibiotics9100635"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"4173","DOI":"10.1172\/JCI72335","article-title":"Host-Microbial Interactions in the Metabolism of Therapeutic and Diet-Derived Xenobiotics","volume":"124","author":"Carmody","year":"2014","journal-title":"J. Clin. Investig."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"20120476","DOI":"10.1098\/rstb.2012.0476","article-title":"Microbial Cytochromes P450: Biodiversity and Biotechnology. Where Do Cytochromes P450 Come from, What Do They Do and What Can They Do for Us?","volume":"368","author":"Kelly","year":"2013","journal-title":"Philos. Trans. R. Soc. B Biol. Sci."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1080\/19490976.2019.1592421","article-title":"Gut Bacteria Signaling to Mitochondria in Intestinal Inflammation and Cancer","volume":"11","author":"Jackson","year":"2020","journal-title":"Gut Microbes"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"1592","DOI":"10.1080\/21505594.2017.1363140","article-title":"Functional and Structural Characteristics of Bacterial Proteins That Bind Host Cytokines","volume":"8","author":"Ihalin","year":"2017","journal-title":"Virulence"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"6290","DOI":"10.1128\/AEM.00871-10","article-title":"Characterization of a Family GH5 Xylanase with Activity on Neutral Oligosaccharides and Evaluation as a Pulp Bleaching Aid","volume":"76","author":"Gallardo","year":"2010","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1007\/s10295-005-0072-1","article-title":"\u03b1-l-Arabinofuranosidases: The Potential Applications in Biotechnology","volume":"33","author":"Numan","year":"2006","journal-title":"J. Ind. Microbiol. Biotechnol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"129848","DOI":"10.1016\/j.bbagen.2021.129848","article-title":"Characterization of Three Bacterial Glycoside Hydrolase Family 9 Endoglucanases with Different Modular Architectures Isolated from a Compost Metagenome","volume":"1865","author":"Henrissat","year":"2021","journal-title":"Biochim. Biophys. Acta BBA\u2014Gen. Subj."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"59","DOI":"10.5458\/jag.jag.JAG-2013_013","article-title":"Characterization of Two \u03b1-1,3-Glucoside Phosphorylases from Clostridium Phytofermentans","volume":"61","author":"Nihira","year":"2014","journal-title":"J. Appl. Glycosci."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1111\/imb.12686","article-title":"Glycosyltransferases: The Multifaceted Enzymatic Regulator in Insects","volume":"30","author":"Nagare","year":"2021","journal-title":"Insect Mol. Biol."},{"key":"ref_81","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":"ref_82","doi-asserted-by":"crossref","first-page":"7618","DOI":"10.1038\/ncomms8618","article-title":"Gut Microbiota Mediate Caffeine Detoxification in the Primary Insect Pest of Coffee","volume":"6","author":"Vega","year":"2015","journal-title":"Nat. Commun."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/11\/8\/1972\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:23:33Z","timestamp":1760127813000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/11\/8\/1972"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,7,31]]},"references-count":82,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2023,8]]}},"alternative-id":["microorganisms11081972"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms11081972","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,7,31]]}}}