A polyphasic taxonomy analysis reveals the presence of an ecotype of Rahnella contaminans associated with the gut of Dendroctonus-bark beetles
Species belonging to the genus Rahnella are dominant members of the core gut bacteriome of Dendroctonus-bark beetles, a group of insects that includes the most destructive agents of pine forest in North and Central America, and Eurasia. From 300 isolates recovered from the gut of these beetles, 10 w...
Main Authors: | , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Frontiers Media S.A.
2023-04-01
|
Series: | Frontiers in Microbiology |
Subjects: | |
Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1171164/full |
_version_ | 1797838579550912512 |
---|---|
author | Flor N. Rivera-Orduña Rosa María Pineda-Mendoza Brenda Vega-Correa María Fernanda López Claudia Cano-Ramírez Xiao Xia Zhang Wen Feng Chen Gerardo Zúñiga |
author_facet | Flor N. Rivera-Orduña Rosa María Pineda-Mendoza Brenda Vega-Correa María Fernanda López Claudia Cano-Ramírez Xiao Xia Zhang Wen Feng Chen Gerardo Zúñiga |
author_sort | Flor N. Rivera-Orduña |
collection | DOAJ |
description | Species belonging to the genus Rahnella are dominant members of the core gut bacteriome of Dendroctonus-bark beetles, a group of insects that includes the most destructive agents of pine forest in North and Central America, and Eurasia. From 300 isolates recovered from the gut of these beetles, 10 were selected to describe an ecotype of Rahnella contaminans. The polyphasic approach conducted with these isolates included phenotypic characteristics, fatty acid analysis, 16S rRNA gene, multilocus sequence analyses (gyrB, rpoB, infB, and atpD genes), and complete genome sequencing of two isolates, ChDrAdgB13 and JaDmexAd06, representative of the studied set. Phenotypic characterization, chemotaxonomic analysis, phylogenetic analyses of the 16S rRNA gene, and multilocus sequence analysis showed that these isolates belonged to Rahnella contaminans. The G + C content of the genome of ChDrAdgB13 (52.8%) and JaDmexAd06 (52.9%) was similar to those from other Rahnella species. The ANI between ChdrAdgB13 and JaDmexAd06 and Rahnella species including R. contaminans, varied from 84.02 to 99.18%. The phylogenomic analysis showed that both strains integrated a consistent and well-defined cluster, together with R. contaminans. A noteworthy observation is the presence of peritrichous flagella and fimbriae in the strains ChDrAdgB13 and JaDmexAd06. The in silico analysis of genes encoding the flagellar system of these strains and Rahnella species showed the presence of flag-1 primary system encoding peritrichous flagella, as well as fimbriae genes from the families type 1, α, β and σ mainly encoding chaperone/usher fimbriae and other uncharacterized families. All this evidence indicates that isolates from the gut of Dendroctonus-bark beetles are an ecotype of R. contaminans, which is dominant and persistent in all developmental stages of these bark beetles and one of the main members of their core gut bacteriome. |
first_indexed | 2024-04-09T15:44:15Z |
format | Article |
id | doaj.art-7843f16389d74b9bad2d1e892526be16 |
institution | Directory Open Access Journal |
issn | 1664-302X |
language | English |
last_indexed | 2024-04-09T15:44:15Z |
publishDate | 2023-04-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Microbiology |
spelling | doaj.art-7843f16389d74b9bad2d1e892526be162023-04-27T05:32:34ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-04-011410.3389/fmicb.2023.11711641171164A polyphasic taxonomy analysis reveals the presence of an ecotype of Rahnella contaminans associated with the gut of Dendroctonus-bark beetlesFlor N. Rivera-Orduña0Rosa María Pineda-Mendoza1Brenda Vega-Correa2María Fernanda López3Claudia Cano-Ramírez4Xiao Xia Zhang5Wen Feng Chen6Gerardo Zúñiga7Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico City, MexicoDepartamento de Zoología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico City, MexicoDepartamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico City, MexicoDepartamento de Zoología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico City, MexicoDepartamento de Zoología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico City, MexicoInstitute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, ChinaState Key Laboratory for Agro-Biotechnology and Ministry of Agriculture Key Lab of Soil Microbiology, College of Biological Sciences, China Agricultural University, Beijing, ChinaDepartamento de Zoología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico City, MexicoSpecies belonging to the genus Rahnella are dominant members of the core gut bacteriome of Dendroctonus-bark beetles, a group of insects that includes the most destructive agents of pine forest in North and Central America, and Eurasia. From 300 isolates recovered from the gut of these beetles, 10 were selected to describe an ecotype of Rahnella contaminans. The polyphasic approach conducted with these isolates included phenotypic characteristics, fatty acid analysis, 16S rRNA gene, multilocus sequence analyses (gyrB, rpoB, infB, and atpD genes), and complete genome sequencing of two isolates, ChDrAdgB13 and JaDmexAd06, representative of the studied set. Phenotypic characterization, chemotaxonomic analysis, phylogenetic analyses of the 16S rRNA gene, and multilocus sequence analysis showed that these isolates belonged to Rahnella contaminans. The G + C content of the genome of ChDrAdgB13 (52.8%) and JaDmexAd06 (52.9%) was similar to those from other Rahnella species. The ANI between ChdrAdgB13 and JaDmexAd06 and Rahnella species including R. contaminans, varied from 84.02 to 99.18%. The phylogenomic analysis showed that both strains integrated a consistent and well-defined cluster, together with R. contaminans. A noteworthy observation is the presence of peritrichous flagella and fimbriae in the strains ChDrAdgB13 and JaDmexAd06. The in silico analysis of genes encoding the flagellar system of these strains and Rahnella species showed the presence of flag-1 primary system encoding peritrichous flagella, as well as fimbriae genes from the families type 1, α, β and σ mainly encoding chaperone/usher fimbriae and other uncharacterized families. All this evidence indicates that isolates from the gut of Dendroctonus-bark beetles are an ecotype of R. contaminans, which is dominant and persistent in all developmental stages of these bark beetles and one of the main members of their core gut bacteriome.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1171164/fullEnterobacteriaceaegut symbiontbark beetlesDendroctonusgut bacteriome |
spellingShingle | Flor N. Rivera-Orduña Rosa María Pineda-Mendoza Brenda Vega-Correa María Fernanda López Claudia Cano-Ramírez Xiao Xia Zhang Wen Feng Chen Gerardo Zúñiga A polyphasic taxonomy analysis reveals the presence of an ecotype of Rahnella contaminans associated with the gut of Dendroctonus-bark beetles Frontiers in Microbiology Enterobacteriaceae gut symbiont bark beetles Dendroctonus gut bacteriome |
title | A polyphasic taxonomy analysis reveals the presence of an ecotype of Rahnella contaminans associated with the gut of Dendroctonus-bark beetles |
title_full | A polyphasic taxonomy analysis reveals the presence of an ecotype of Rahnella contaminans associated with the gut of Dendroctonus-bark beetles |
title_fullStr | A polyphasic taxonomy analysis reveals the presence of an ecotype of Rahnella contaminans associated with the gut of Dendroctonus-bark beetles |
title_full_unstemmed | A polyphasic taxonomy analysis reveals the presence of an ecotype of Rahnella contaminans associated with the gut of Dendroctonus-bark beetles |
title_short | A polyphasic taxonomy analysis reveals the presence of an ecotype of Rahnella contaminans associated with the gut of Dendroctonus-bark beetles |
title_sort | polyphasic taxonomy analysis reveals the presence of an ecotype of rahnella contaminans associated with the gut of dendroctonus bark beetles |
topic | Enterobacteriaceae gut symbiont bark beetles Dendroctonus gut bacteriome |
url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1171164/full |
work_keys_str_mv | AT flornriveraorduna apolyphasictaxonomyanalysisrevealsthepresenceofanecotypeofrahnellacontaminansassociatedwiththegutofdendroctonusbarkbeetles AT rosamariapinedamendoza apolyphasictaxonomyanalysisrevealsthepresenceofanecotypeofrahnellacontaminansassociatedwiththegutofdendroctonusbarkbeetles AT brendavegacorrea apolyphasictaxonomyanalysisrevealsthepresenceofanecotypeofrahnellacontaminansassociatedwiththegutofdendroctonusbarkbeetles AT mariafernandalopez apolyphasictaxonomyanalysisrevealsthepresenceofanecotypeofrahnellacontaminansassociatedwiththegutofdendroctonusbarkbeetles AT claudiacanoramirez apolyphasictaxonomyanalysisrevealsthepresenceofanecotypeofrahnellacontaminansassociatedwiththegutofdendroctonusbarkbeetles AT xiaoxiazhang apolyphasictaxonomyanalysisrevealsthepresenceofanecotypeofrahnellacontaminansassociatedwiththegutofdendroctonusbarkbeetles AT wenfengchen apolyphasictaxonomyanalysisrevealsthepresenceofanecotypeofrahnellacontaminansassociatedwiththegutofdendroctonusbarkbeetles AT gerardozuniga apolyphasictaxonomyanalysisrevealsthepresenceofanecotypeofrahnellacontaminansassociatedwiththegutofdendroctonusbarkbeetles AT flornriveraorduna polyphasictaxonomyanalysisrevealsthepresenceofanecotypeofrahnellacontaminansassociatedwiththegutofdendroctonusbarkbeetles AT rosamariapinedamendoza polyphasictaxonomyanalysisrevealsthepresenceofanecotypeofrahnellacontaminansassociatedwiththegutofdendroctonusbarkbeetles AT brendavegacorrea polyphasictaxonomyanalysisrevealsthepresenceofanecotypeofrahnellacontaminansassociatedwiththegutofdendroctonusbarkbeetles AT mariafernandalopez polyphasictaxonomyanalysisrevealsthepresenceofanecotypeofrahnellacontaminansassociatedwiththegutofdendroctonusbarkbeetles AT claudiacanoramirez polyphasictaxonomyanalysisrevealsthepresenceofanecotypeofrahnellacontaminansassociatedwiththegutofdendroctonusbarkbeetles AT xiaoxiazhang polyphasictaxonomyanalysisrevealsthepresenceofanecotypeofrahnellacontaminansassociatedwiththegutofdendroctonusbarkbeetles AT wenfengchen polyphasictaxonomyanalysisrevealsthepresenceofanecotypeofrahnellacontaminansassociatedwiththegutofdendroctonusbarkbeetles AT gerardozuniga polyphasictaxonomyanalysisrevealsthepresenceofanecotypeofrahnellacontaminansassociatedwiththegutofdendroctonusbarkbeetles |