Cargando…
Genomic analysis of novel Yarrowia-like yeast symbionts associated with the carrion-feeding burying beetle Nicrophorus vespilloides
BACKGROUND: Mutualistic interactions with microbes can help insects adapt to extreme environments and unusual diets. An intriguing example is the burying beetle Nicrophorus vespilloides, which feeds and reproduces on small vertebrate carcasses. Its fungal microbiome is dominated by yeasts that poten...
Autores principales: | , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2021
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8091737/ https://www.ncbi.nlm.nih.gov/pubmed/33941076 http://dx.doi.org/10.1186/s12864-021-07597-z |
_version_ | 1783687538932711424 |
---|---|
author | Brinkrolf, Karina Shukla, Shantanu P. Griep, Sven Rupp, Oliver Heise, Philipp Goesmann, Alexander Heckel, David G. Vogel, Heiko Vilcinskas, Andreas |
author_facet | Brinkrolf, Karina Shukla, Shantanu P. Griep, Sven Rupp, Oliver Heise, Philipp Goesmann, Alexander Heckel, David G. Vogel, Heiko Vilcinskas, Andreas |
author_sort | Brinkrolf, Karina |
collection | PubMed |
description | BACKGROUND: Mutualistic interactions with microbes can help insects adapt to extreme environments and unusual diets. An intriguing example is the burying beetle Nicrophorus vespilloides, which feeds and reproduces on small vertebrate carcasses. Its fungal microbiome is dominated by yeasts that potentially facilitate carcass utilization by producing digestive enzymes, eliminating cadaver-associated toxic volatiles (that would otherwise attract competitors), and releasing antimicrobials to sanitize the microenvironment. Some of these yeasts are closely related to the biotechnologically important species Yarrowia lipolytica. RESULTS: To investigate the roles of these Yarrowia-like yeast (YLY) strains in more detail, we selected five strains from two different phylogenetic clades for third-generation sequencing and genome analysis. The first clade, represented by strain B02, has a 20-Mb genome containing ~ 6400 predicted protein-coding genes. The second clade, represented by strain C11, has a 25-Mb genome containing ~ 6300 predicted protein-coding genes, and extensive intraspecific variability within the ITS–D1/D2 rDNA region commonly used for species assignments. Phenotypic microarray analysis revealed that both YLY strains were able to utilize a diverse range of carbon and nitrogen sources (including microbial metabolites associated with putrefaction), and can grow in environments with extreme pH and salt concentrations. CONCLUSIONS: The genomic characterization of five yeast strains isolated from N. vespilloides resulted in the identification of strains potentially representing new YLY species. Given their abundance in the beetle hindgut, and dominant growth on beetle-prepared carcasses, the analysis of these strains has revealed the genetic basis of a potential symbiotic relationship between yeasts and burying beetles that facilitates carcass digestion and preservation. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07597-z. |
format | Online Article Text |
id | pubmed-8091737 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-80917372021-05-04 Genomic analysis of novel Yarrowia-like yeast symbionts associated with the carrion-feeding burying beetle Nicrophorus vespilloides Brinkrolf, Karina Shukla, Shantanu P. Griep, Sven Rupp, Oliver Heise, Philipp Goesmann, Alexander Heckel, David G. Vogel, Heiko Vilcinskas, Andreas BMC Genomics Research Article BACKGROUND: Mutualistic interactions with microbes can help insects adapt to extreme environments and unusual diets. An intriguing example is the burying beetle Nicrophorus vespilloides, which feeds and reproduces on small vertebrate carcasses. Its fungal microbiome is dominated by yeasts that potentially facilitate carcass utilization by producing digestive enzymes, eliminating cadaver-associated toxic volatiles (that would otherwise attract competitors), and releasing antimicrobials to sanitize the microenvironment. Some of these yeasts are closely related to the biotechnologically important species Yarrowia lipolytica. RESULTS: To investigate the roles of these Yarrowia-like yeast (YLY) strains in more detail, we selected five strains from two different phylogenetic clades for third-generation sequencing and genome analysis. The first clade, represented by strain B02, has a 20-Mb genome containing ~ 6400 predicted protein-coding genes. The second clade, represented by strain C11, has a 25-Mb genome containing ~ 6300 predicted protein-coding genes, and extensive intraspecific variability within the ITS–D1/D2 rDNA region commonly used for species assignments. Phenotypic microarray analysis revealed that both YLY strains were able to utilize a diverse range of carbon and nitrogen sources (including microbial metabolites associated with putrefaction), and can grow in environments with extreme pH and salt concentrations. CONCLUSIONS: The genomic characterization of five yeast strains isolated from N. vespilloides resulted in the identification of strains potentially representing new YLY species. Given their abundance in the beetle hindgut, and dominant growth on beetle-prepared carcasses, the analysis of these strains has revealed the genetic basis of a potential symbiotic relationship between yeasts and burying beetles that facilitates carcass digestion and preservation. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07597-z. BioMed Central 2021-05-03 /pmc/articles/PMC8091737/ /pubmed/33941076 http://dx.doi.org/10.1186/s12864-021-07597-z Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Article Brinkrolf, Karina Shukla, Shantanu P. Griep, Sven Rupp, Oliver Heise, Philipp Goesmann, Alexander Heckel, David G. Vogel, Heiko Vilcinskas, Andreas Genomic analysis of novel Yarrowia-like yeast symbionts associated with the carrion-feeding burying beetle Nicrophorus vespilloides |
title | Genomic analysis of novel Yarrowia-like yeast symbionts associated with the carrion-feeding burying beetle Nicrophorus vespilloides |
title_full | Genomic analysis of novel Yarrowia-like yeast symbionts associated with the carrion-feeding burying beetle Nicrophorus vespilloides |
title_fullStr | Genomic analysis of novel Yarrowia-like yeast symbionts associated with the carrion-feeding burying beetle Nicrophorus vespilloides |
title_full_unstemmed | Genomic analysis of novel Yarrowia-like yeast symbionts associated with the carrion-feeding burying beetle Nicrophorus vespilloides |
title_short | Genomic analysis of novel Yarrowia-like yeast symbionts associated with the carrion-feeding burying beetle Nicrophorus vespilloides |
title_sort | genomic analysis of novel yarrowia-like yeast symbionts associated with the carrion-feeding burying beetle nicrophorus vespilloides |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8091737/ https://www.ncbi.nlm.nih.gov/pubmed/33941076 http://dx.doi.org/10.1186/s12864-021-07597-z |
work_keys_str_mv | AT brinkrolfkarina genomicanalysisofnovelyarrowialikeyeastsymbiontsassociatedwiththecarrionfeedingburyingbeetlenicrophorusvespilloides AT shuklashantanup genomicanalysisofnovelyarrowialikeyeastsymbiontsassociatedwiththecarrionfeedingburyingbeetlenicrophorusvespilloides AT griepsven genomicanalysisofnovelyarrowialikeyeastsymbiontsassociatedwiththecarrionfeedingburyingbeetlenicrophorusvespilloides AT ruppoliver genomicanalysisofnovelyarrowialikeyeastsymbiontsassociatedwiththecarrionfeedingburyingbeetlenicrophorusvespilloides AT heisephilipp genomicanalysisofnovelyarrowialikeyeastsymbiontsassociatedwiththecarrionfeedingburyingbeetlenicrophorusvespilloides AT goesmannalexander genomicanalysisofnovelyarrowialikeyeastsymbiontsassociatedwiththecarrionfeedingburyingbeetlenicrophorusvespilloides AT heckeldavidg genomicanalysisofnovelyarrowialikeyeastsymbiontsassociatedwiththecarrionfeedingburyingbeetlenicrophorusvespilloides AT vogelheiko genomicanalysisofnovelyarrowialikeyeastsymbiontsassociatedwiththecarrionfeedingburyingbeetlenicrophorusvespilloides AT vilcinskasandreas genomicanalysisofnovelyarrowialikeyeastsymbiontsassociatedwiththecarrionfeedingburyingbeetlenicrophorusvespilloides |