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

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

Research output: Contribution to JournalArticleAcademicpeer-review

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.

Original languageEnglish
Article number493
JournalBMC Genomics
Volume18
DOIs
Publication statusPublished - 28 Jun 2017

Fingerprint

Candida
Soil
Genome
Multigene Family
Wolbachia
Genes
Arthropods
Life Style
Ecotoxicology
Physiological Adaptation
Horizontal Gene Transfer
Homeobox Genes
Ecology
Consensus
Carbohydrates
Anti-Bacterial Agents

Keywords

  • Carbohydrate metabolism
  • Collembola
  • Gene family expansions
  • Genome collinearity
  • Horizontal gene transfer
  • Hox genes
  • Intragenomic rearrangement
  • Palindrome

Cite this

Faddeeva-Vakhrusheva, A., Kraaijeveld, K., Derks, M. F. L., Anvar, S. Y., Agamennone, V., Suring, W., ... Roelofs, D. (2017). Coping with living in the soil: the genome of the parthenogenetic springtail Folsomia candida. BMC Genomics, 18, [493]. https://doi.org/10.1186/s12864-017-3852-x
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. In: BMC Genomics. 2017 ; Vol. 18.
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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.",
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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.

In: BMC Genomics, Vol. 18, 493, 28.06.2017.

Research output: Contribution to JournalArticleAcademicpeer-review

TY - JOUR

T1 - Coping with living in the soil:

T2 - the genome of the parthenogenetic springtail Folsomia candida

AU - Faddeeva-Vakhrusheva, Anna

AU - Kraaijeveld, Ken

AU - Derks, Martijn F L

AU - Anvar, Seyed Yahya

AU - Agamennone, Valeria

AU - Suring, Wouter

AU - Kampfraath, Andries A.

AU - Ellers, Jacintha

AU - Le Ngoc, Giang

AU - van Gestel, Cornelis A.M.

AU - Mariën, Janine

AU - Smit, Sandra

AU - van Straalen, Nico M.

AU - Roelofs, Dick

PY - 2017/6/28

Y1 - 2017/6/28

N2 - 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.

AB - 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.

KW - Carbohydrate metabolism

KW - Collembola

KW - Gene family expansions

KW - Genome collinearity

KW - Horizontal gene transfer

KW - Hox genes

KW - Intragenomic rearrangement

KW - Palindrome

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Faddeeva-Vakhrusheva A, Kraaijeveld K, Derks MFL, Anvar SY, Agamennone V, Suring W et al. Coping with living in the soil: the genome of the parthenogenetic springtail Folsomia candida. BMC Genomics. 2017 Jun 28;18. 493. https://doi.org/10.1186/s12864-017-3852-x