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Coping with living in the soil: the genome of the parthenogenetic springtail Folsomia candida

BACKGROUND: Folsomia candida is a model in soil biology, belonging to the family of Isotomidae, subclass Collembola. It reproduces parthenogenetically in the presence of Wolbachia, and exhibits remarkable physiological adaptations to stress. To better understand these features and adaptations to lif...

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Autores principales: Faddeeva-Vakhrusheva, Anna, Kraaijeveld, Ken, Derks, Martijn F. L., Anvar, Seyed Yahya, Agamennone, Valeria, Suring, Wouter, Kampfraath, Andries A., Ellers, Jacintha, Le Ngoc, Giang, van Gestel, Cornelis A. M., Mariën, Janine, Smit, Sandra, van Straalen, Nico M., Roelofs, Dick
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5490193/
https://www.ncbi.nlm.nih.gov/pubmed/28659179
http://dx.doi.org/10.1186/s12864-017-3852-x
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author Faddeeva-Vakhrusheva, Anna
Kraaijeveld, Ken
Derks, Martijn F. L.
Anvar, Seyed Yahya
Agamennone, Valeria
Suring, Wouter
Kampfraath, Andries A.
Ellers, Jacintha
Le Ngoc, Giang
van Gestel, Cornelis A. M.
Mariën, Janine
Smit, Sandra
van Straalen, Nico M.
Roelofs, Dick
author_facet Faddeeva-Vakhrusheva, Anna
Kraaijeveld, Ken
Derks, Martijn F. L.
Anvar, Seyed Yahya
Agamennone, Valeria
Suring, Wouter
Kampfraath, Andries A.
Ellers, Jacintha
Le Ngoc, Giang
van Gestel, Cornelis A. M.
Mariën, Janine
Smit, Sandra
van Straalen, Nico M.
Roelofs, Dick
author_sort Faddeeva-Vakhrusheva, Anna
collection PubMed
description BACKGROUND: Folsomia candida is a model in soil biology, belonging to the family of Isotomidae, subclass Collembola. It reproduces parthenogenetically in the presence of Wolbachia, and exhibits remarkable physiological adaptations to stress. To better understand these features and adaptations to life in the soil, we studied its genome in the context of its parthenogenetic lifestyle. RESULTS: We applied Pacific Bioscience sequencing and assembly to generate a reference genome for F. candida of 221.7 Mbp, comprising only 162 scaffolds. The complete genome of its endosymbiont Wolbachia, was also assembled and turned out to be the largest strain identified so far. Substantial gene family expansions and lineage-specific gene clusters were linked to stress response. A large number of genes (809) were acquired by horizontal gene transfer. A substantial fraction of these genes are involved in lignocellulose degradation. Also, the presence of genes involved in antibiotic biosynthesis was confirmed. Intra-genomic rearrangements of collinear gene clusters were observed, of which 11 were organized as palindromes. The Hox gene cluster of F. candida showed major rearrangements compared to arthropod consensus cluster, resulting in a disorganized cluster. CONCLUSIONS: The expansion of stress response gene families suggests that stress defense was important to facilitate colonization of soils. The large number of HGT genes related to lignocellulose degradation could be beneficial to unlock carbohydrate sources in soil, especially those contained in decaying plant and fungal organic matter. Intra- as well as inter-scaffold duplications of gene clusters may be a consequence of its parthenogenetic lifestyle. This high quality genome will be instrumental for evolutionary biologists investigating deep phylogenetic lineages among arthropods and will provide the basis for a more mechanistic understanding in soil ecology and ecotoxicology. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-017-3852-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-54901932017-06-30 Coping with living in the soil: the genome of the parthenogenetic springtail Folsomia candida Faddeeva-Vakhrusheva, Anna Kraaijeveld, Ken Derks, Martijn F. L. Anvar, Seyed Yahya Agamennone, Valeria Suring, Wouter Kampfraath, Andries A. Ellers, Jacintha Le Ngoc, Giang van Gestel, Cornelis A. M. Mariën, Janine Smit, Sandra van Straalen, Nico M. Roelofs, Dick BMC Genomics Research Article BACKGROUND: Folsomia candida is a model in soil biology, belonging to the family of Isotomidae, subclass Collembola. It reproduces parthenogenetically in the presence of Wolbachia, and exhibits remarkable physiological adaptations to stress. To better understand these features and adaptations to life in the soil, we studied its genome in the context of its parthenogenetic lifestyle. RESULTS: We applied Pacific Bioscience sequencing and assembly to generate a reference genome for F. candida of 221.7 Mbp, comprising only 162 scaffolds. The complete genome of its endosymbiont Wolbachia, was also assembled and turned out to be the largest strain identified so far. Substantial gene family expansions and lineage-specific gene clusters were linked to stress response. A large number of genes (809) were acquired by horizontal gene transfer. A substantial fraction of these genes are involved in lignocellulose degradation. Also, the presence of genes involved in antibiotic biosynthesis was confirmed. Intra-genomic rearrangements of collinear gene clusters were observed, of which 11 were organized as palindromes. The Hox gene cluster of F. candida showed major rearrangements compared to arthropod consensus cluster, resulting in a disorganized cluster. CONCLUSIONS: The expansion of stress response gene families suggests that stress defense was important to facilitate colonization of soils. The large number of HGT genes related to lignocellulose degradation could be beneficial to unlock carbohydrate sources in soil, especially those contained in decaying plant and fungal organic matter. Intra- as well as inter-scaffold duplications of gene clusters may be a consequence of its parthenogenetic lifestyle. This high quality genome will be instrumental for evolutionary biologists investigating deep phylogenetic lineages among arthropods and will provide the basis for a more mechanistic understanding in soil ecology and ecotoxicology. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-017-3852-x) contains supplementary material, which is available to authorized users. BioMed Central 2017-06-28 /pmc/articles/PMC5490193/ /pubmed/28659179 http://dx.doi.org/10.1186/s12864-017-3852-x Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Faddeeva-Vakhrusheva, Anna
Kraaijeveld, Ken
Derks, Martijn F. L.
Anvar, Seyed Yahya
Agamennone, Valeria
Suring, Wouter
Kampfraath, Andries A.
Ellers, Jacintha
Le Ngoc, Giang
van Gestel, Cornelis A. M.
Mariën, Janine
Smit, Sandra
van Straalen, Nico M.
Roelofs, Dick
Coping with living in the soil: the genome of the parthenogenetic springtail Folsomia candida
title Coping with living in the soil: the genome of the parthenogenetic springtail Folsomia candida
title_full Coping with living in the soil: the genome of the parthenogenetic springtail Folsomia candida
title_fullStr Coping with living in the soil: the genome of the parthenogenetic springtail Folsomia candida
title_full_unstemmed Coping with living in the soil: the genome of the parthenogenetic springtail Folsomia candida
title_short Coping with living in the soil: the genome of the parthenogenetic springtail Folsomia candida
title_sort coping with living in the soil: the genome of the parthenogenetic springtail folsomia candida
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5490193/
https://www.ncbi.nlm.nih.gov/pubmed/28659179
http://dx.doi.org/10.1186/s12864-017-3852-x
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