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

Abstract 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 adaptation...

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Main Authors: Anna Faddeeva-Vakhrusheva, Ken Kraaijeveld, Martijn F. L. Derks, Seyed Yahya Anvar, Valeria Agamennone, Wouter Suring, Andries A. Kampfraath, Jacintha Ellers, Giang Le Ngoc, Cornelis A. M. van Gestel, Janine Mariën, Sandra Smit, Nico M. van Straalen, Dick Roelofs
Format: Article
Language:English
Published: BMC 2017-06-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-017-3852-x
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spelling doaj-6497bf36c83d4c6a8dbae14e60e945212020-11-25T00:39:57ZengBMCBMC Genomics1471-21642017-06-0118111410.1186/s12864-017-3852-xCoping with living in the soil: the genome of the parthenogenetic springtail Folsomia candidaAnna Faddeeva-Vakhrusheva0Ken Kraaijeveld1Martijn F. L. Derks2Seyed Yahya Anvar3Valeria Agamennone4Wouter Suring5Andries A. Kampfraath6Jacintha Ellers7Giang Le Ngoc8Cornelis A. M. van Gestel9Janine Mariën10Sandra Smit11Nico M. van Straalen12Dick Roelofs13Department of Ecological Science, Vrije Universiteit AmsterdamDepartment of Ecological Science, Vrije Universiteit AmsterdamDepartment of Animal Sciences, Animal Breeding and Genetics, Wageningen UniversityDepartment of Human Genetics, Leiden University Medical CenterDepartment of Ecological Science, Vrije Universiteit AmsterdamDepartment of Ecological Science, Vrije Universiteit AmsterdamDepartment of Ecological Science, Vrije Universiteit AmsterdamDepartment of Ecological Science, Vrije Universiteit AmsterdamDepartment of Ecological Science, Vrije Universiteit AmsterdamDepartment of Ecological Science, Vrije Universiteit AmsterdamDepartment of Ecological Science, Vrije Universiteit AmsterdamDepartment of Plant Sciences, Bioinformatics Group, Wageningen UniversityDepartment of Ecological Science, Vrije Universiteit AmsterdamDepartment of Ecological Science, Vrije Universiteit AmsterdamAbstract 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.http://link.springer.com/article/10.1186/s12864-017-3852-xCollembolaIntragenomic rearrangementGene family expansionsHox genesHorizontal gene transferGenome collinearity
collection DOAJ
language English
format Article
sources DOAJ
author Anna Faddeeva-Vakhrusheva
Ken Kraaijeveld
Martijn F. L. Derks
Seyed Yahya Anvar
Valeria Agamennone
Wouter Suring
Andries A. Kampfraath
Jacintha Ellers
Giang Le Ngoc
Cornelis A. M. van Gestel
Janine Mariën
Sandra Smit
Nico M. van Straalen
Dick Roelofs
spellingShingle Anna Faddeeva-Vakhrusheva
Ken Kraaijeveld
Martijn F. L. Derks
Seyed Yahya Anvar
Valeria Agamennone
Wouter Suring
Andries A. Kampfraath
Jacintha Ellers
Giang Le Ngoc
Cornelis A. M. van Gestel
Janine Mariën
Sandra Smit
Nico M. van Straalen
Dick Roelofs
Coping with living in the soil: the genome of the parthenogenetic springtail Folsomia candida
BMC Genomics
Collembola
Intragenomic rearrangement
Gene family expansions
Hox genes
Horizontal gene transfer
Genome collinearity
author_facet Anna Faddeeva-Vakhrusheva
Ken Kraaijeveld
Martijn F. L. Derks
Seyed Yahya Anvar
Valeria Agamennone
Wouter Suring
Andries A. Kampfraath
Jacintha Ellers
Giang Le Ngoc
Cornelis A. M. van Gestel
Janine Mariën
Sandra Smit
Nico M. van Straalen
Dick Roelofs
author_sort Anna Faddeeva-Vakhrusheva
title 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_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_sort coping with living in the soil: the genome of the parthenogenetic springtail folsomia candida
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2017-06-01
description Abstract 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.
topic Collembola
Intragenomic rearrangement
Gene family expansions
Hox genes
Horizontal gene transfer
Genome collinearity
url http://link.springer.com/article/10.1186/s12864-017-3852-x
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