The Skin Microbiome of the Neotropical Frog Craugastor fitzingeri: Inferring Potential Bacterial-Host-Pathogen Interactions From Metagenomic Data
Skin symbiotic bacteria on amphibians can play a role in protecting their host against pathogens. Chytridiomycosis, the disease caused by Batrachochytrium dendrobatidis, Bd, has caused dramatic population declines and extinctions of amphibians worldwide. Anti-Bd bacteria from amphibian skin have bee...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2018-03-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | http://journal.frontiersin.org/article/10.3389/fmicb.2018.00466/full |
| _version_ | 1818159241189392384 |
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| author | Eria A. Rebollar Ana Gutiérrez-Preciado Cecilia Noecker Alexander Eng Myra C. Hughey Daniel Medina Jenifer B. Walke Elhanan Borenstein Elhanan Borenstein Elhanan Borenstein Roderick V. Jensen Lisa K. Belden Lisa K. Belden Reid N. Harris Reid N. Harris |
| author_facet | Eria A. Rebollar Ana Gutiérrez-Preciado Cecilia Noecker Alexander Eng Myra C. Hughey Daniel Medina Jenifer B. Walke Elhanan Borenstein Elhanan Borenstein Elhanan Borenstein Roderick V. Jensen Lisa K. Belden Lisa K. Belden Reid N. Harris Reid N. Harris |
| author_sort | Eria A. Rebollar |
| collection | DOAJ |
| description | Skin symbiotic bacteria on amphibians can play a role in protecting their host against pathogens. Chytridiomycosis, the disease caused by Batrachochytrium dendrobatidis, Bd, has caused dramatic population declines and extinctions of amphibians worldwide. Anti-Bd bacteria from amphibian skin have been cultured, and skin bacterial communities have been described through 16S rRNA gene amplicon sequencing. Here, we present a shotgun metagenomic analysis of skin bacterial communities from a Neotropical frog, Craugastor fitzingeri. We sequenced the metagenome of six frogs from two different sites in Panamá: three frogs from Soberanía (Sob), a Bd-endemic site, and three frogs from Serranía del Sapo (Sapo), a Bd-naïve site. We described the taxonomic composition of skin microbiomes and found that Pseudomonas was a major component of these communities. We also identified that Sob communities were enriched in Actinobacteria while Sapo communities were enriched in Gammaproteobacteria. We described gene abundances within the main functional classes and found genes enriched either in Sapo or Sob. We then focused our study on five functional classes of genes: biosynthesis of secondary metabolites, metabolism of terpenoids and polyketides, membrane transport, cellular communication and antimicrobial drug resistance. These gene classes are potentially involved in bacterial communication, bacterial-host and bacterial-pathogen interactions among other functions. We found that C. fitzingeri metagenomes have a wide array of genes that code for secondary metabolites, including antibiotics and bacterial toxins, which may be involved in bacterial communication, but could also have a defensive role against pathogens. Several genes involved in bacterial communication and bacterial-host interactions, such as biofilm formation and bacterial secretion systems were found. We identified specific genes and pathways enriched at the different sites and determined that gene co-occurrence networks differed between sites. Our results suggest that skin microbiomes are composed of distinct bacterial taxa with a wide range of metabolic capabilities involved in bacterial defense and communication. Differences in taxonomic composition and pathway enrichments suggest that skin microbiomes from different sites have unique functional properties. This study strongly supports the need for shotgun metagenomic analyses to describe the functional capacities of skin microbiomes and to tease apart their role in host defense against pathogens. |
| first_indexed | 2024-12-11T15:42:51Z |
| format | Article |
| id | doaj.art-e4b4e600519846e2b16042b0951694e5 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-11T15:42:51Z |
| publishDate | 2018-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-e4b4e600519846e2b16042b0951694e52022-12-22T00:59:46ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-03-01910.3389/fmicb.2018.00466327185The Skin Microbiome of the Neotropical Frog Craugastor fitzingeri: Inferring Potential Bacterial-Host-Pathogen Interactions From Metagenomic DataEria A. Rebollar0Ana Gutiérrez-Preciado1Cecilia Noecker2Alexander Eng3Myra C. Hughey4Daniel Medina5Jenifer B. Walke6Elhanan Borenstein7Elhanan Borenstein8Elhanan Borenstein9Roderick V. Jensen10Lisa K. Belden11Lisa K. Belden12Reid N. Harris13Reid N. Harris14Department of Biology, James Madison University, Harrisonburg, VA, United StatesUnité d'Ecologie, Systématique et Evolution, Université Paris-Sud, Paris, FranceDepartment of Genome Sciences, University of Washington, Seattle, WA, United StatesDepartment of Genome Sciences, University of Washington, Seattle, WA, United StatesDepartment of Biological Sciences, Virginia Tech, Blacksburg, VA, United StatesDepartment of Biological Sciences, Virginia Tech, Blacksburg, VA, United StatesDepartment of Biological Sciences, Virginia Tech, Blacksburg, VA, United StatesDepartment of Genome Sciences, University of Washington, Seattle, WA, United StatesDepartment of Computer Science and Engineering, University of Washington, Seattle, WA, United StatesSanta Fe Institute, Santa Fe, NM, United StatesDepartment of Biological Sciences, Virginia Tech, Blacksburg, VA, United StatesDepartment of Biological Sciences, Virginia Tech, Blacksburg, VA, United StatesSmithsonian Tropical Research Institution, Panama City, PanamaDepartment of Biology, James Madison University, Harrisonburg, VA, United StatesAmphibian Survival Alliance, London, United KingdomSkin symbiotic bacteria on amphibians can play a role in protecting their host against pathogens. Chytridiomycosis, the disease caused by Batrachochytrium dendrobatidis, Bd, has caused dramatic population declines and extinctions of amphibians worldwide. Anti-Bd bacteria from amphibian skin have been cultured, and skin bacterial communities have been described through 16S rRNA gene amplicon sequencing. Here, we present a shotgun metagenomic analysis of skin bacterial communities from a Neotropical frog, Craugastor fitzingeri. We sequenced the metagenome of six frogs from two different sites in Panamá: three frogs from Soberanía (Sob), a Bd-endemic site, and three frogs from Serranía del Sapo (Sapo), a Bd-naïve site. We described the taxonomic composition of skin microbiomes and found that Pseudomonas was a major component of these communities. We also identified that Sob communities were enriched in Actinobacteria while Sapo communities were enriched in Gammaproteobacteria. We described gene abundances within the main functional classes and found genes enriched either in Sapo or Sob. We then focused our study on five functional classes of genes: biosynthesis of secondary metabolites, metabolism of terpenoids and polyketides, membrane transport, cellular communication and antimicrobial drug resistance. These gene classes are potentially involved in bacterial communication, bacterial-host and bacterial-pathogen interactions among other functions. We found that C. fitzingeri metagenomes have a wide array of genes that code for secondary metabolites, including antibiotics and bacterial toxins, which may be involved in bacterial communication, but could also have a defensive role against pathogens. Several genes involved in bacterial communication and bacterial-host interactions, such as biofilm formation and bacterial secretion systems were found. We identified specific genes and pathways enriched at the different sites and determined that gene co-occurrence networks differed between sites. Our results suggest that skin microbiomes are composed of distinct bacterial taxa with a wide range of metabolic capabilities involved in bacterial defense and communication. Differences in taxonomic composition and pathway enrichments suggest that skin microbiomes from different sites have unique functional properties. This study strongly supports the need for shotgun metagenomic analyses to describe the functional capacities of skin microbiomes and to tease apart their role in host defense against pathogens.http://journal.frontiersin.org/article/10.3389/fmicb.2018.00466/fullskin microbiomeshotgun metagenomicshost-bacteria interactionsamphibiansBatrachochytrium dendrobatidis |
| spellingShingle | Eria A. Rebollar Ana Gutiérrez-Preciado Cecilia Noecker Alexander Eng Myra C. Hughey Daniel Medina Jenifer B. Walke Elhanan Borenstein Elhanan Borenstein Elhanan Borenstein Roderick V. Jensen Lisa K. Belden Lisa K. Belden Reid N. Harris Reid N. Harris The Skin Microbiome of the Neotropical Frog Craugastor fitzingeri: Inferring Potential Bacterial-Host-Pathogen Interactions From Metagenomic Data Frontiers in Microbiology skin microbiome shotgun metagenomics host-bacteria interactions amphibians Batrachochytrium dendrobatidis |
| title | The Skin Microbiome of the Neotropical Frog Craugastor fitzingeri: Inferring Potential Bacterial-Host-Pathogen Interactions From Metagenomic Data |
| title_full | The Skin Microbiome of the Neotropical Frog Craugastor fitzingeri: Inferring Potential Bacterial-Host-Pathogen Interactions From Metagenomic Data |
| title_fullStr | The Skin Microbiome of the Neotropical Frog Craugastor fitzingeri: Inferring Potential Bacterial-Host-Pathogen Interactions From Metagenomic Data |
| title_full_unstemmed | The Skin Microbiome of the Neotropical Frog Craugastor fitzingeri: Inferring Potential Bacterial-Host-Pathogen Interactions From Metagenomic Data |
| title_short | The Skin Microbiome of the Neotropical Frog Craugastor fitzingeri: Inferring Potential Bacterial-Host-Pathogen Interactions From Metagenomic Data |
| title_sort | skin microbiome of the neotropical frog craugastor fitzingeri inferring potential bacterial host pathogen interactions from metagenomic data |
| topic | skin microbiome shotgun metagenomics host-bacteria interactions amphibians Batrachochytrium dendrobatidis |
| url | http://journal.frontiersin.org/article/10.3389/fmicb.2018.00466/full |
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