Exploring the genomic traits of fungus-feeding bacterial genus Collimonas

Chunxu Song, Ruth Schmidt, Victor de Jager, Dorota Krzyzanowska, Esmer Jongedijk, Katarina Cankar, Jules Beekwilder, Anouk van Veen, Wietse de Boer, Johannes A. van Veen, Paolina Garbeva

Research output: Contribution to journalArticleAcademicpeer-review

21 Citations (Scopus)

Abstract

Background: Collimonas is a genus belonging to the class of Betaproteobacteria and consists mostly of soil bacteria with the ability to exploit living fungi as food source (mycophagy). Collimonas strains differ in a range of activities, including swimming motility, quorum sensing, extracellular protease activity, siderophore production, and antimicrobial activities. Results: In order to reveal ecological traits possibly related to Collimonas lifestyle and secondary metabolites production, we performed a comparative genomics analysis based on whole-genome sequencing of six strains representing 3 recognized species. The analysis revealed that the core genome represents 43.1 to 52.7 % of the genomes of the six individual strains. These include genes coding for extracellular enzymes (chitinase, peptidase, phospholipase), iron acquisition and type II secretion systems. In the variable genome, differences were found in genes coding for secondary metabolites (e.g. tripropeptin A and volatile terpenes), several unknown orphan polyketide synthase-nonribosomal peptide synthetase (PKS-NRPS), nonribosomal peptide synthetase (NRPS) gene clusters, a new lipopeptide and type III and type VI secretion systems. Potential roles of the latter genes in the interaction with other organisms were investigated. Mutation of a gene involved in tripropeptin A biosynthesis strongly reduced the antibacterial activity against Staphylococcus aureus, while disruption of a gene involved in the biosynthesis of the new lipopeptide had a large effect on the antifungal/oomycetal activities. Conclusions: Overall our results indicated that Collimonas genomes harbour many genes encoding for novel enzymes and secondary metabolites (including terpenes) important for interactions with other organisms and revealed genomic plasticity, which reflect the behaviour, antimicrobial activity and lifestylesof Collimonas spp.

LanguageEnglish
Article number1103
JournalBMC Genomics
Volume16
Issue number1
DOIs
Publication statusPublished - 24 Dec 2015

Fingerprint

Fungi
Genome
Peptide Synthases
Genes
Lipopeptides
Terpenes
Peptide Hydrolases
Betaproteobacteria
Polyketide Synthases
Siderophores
Quorum Sensing
Chitinases
Orphaned Children
Aptitude
Phospholipases
Enzymes
Multigene Family
Genomics
Staphylococcus aureus
Life Style

Keywords

  • Collimonas
  • Comparative genomics
  • Secondary metabolites
  • Terpenes

Cite this

Song, C., Schmidt, R., de Jager, V., Krzyzanowska, D., Jongedijk, E., Cankar, K., ... Garbeva, P. (2015). Exploring the genomic traits of fungus-feeding bacterial genus Collimonas. BMC Genomics, 16(1), [1103]. https://doi.org/10.1186/s12864-015-2289-3
Song, Chunxu ; Schmidt, Ruth ; de Jager, Victor ; Krzyzanowska, Dorota ; Jongedijk, Esmer ; Cankar, Katarina ; Beekwilder, Jules ; van Veen, Anouk ; de Boer, Wietse ; van Veen, Johannes A. ; Garbeva, Paolina. / Exploring the genomic traits of fungus-feeding bacterial genus Collimonas. In: BMC Genomics. 2015 ; Vol. 16, No. 1.
@article{343d47e79ace4622ad93965eed1e87ae,
title = "Exploring the genomic traits of fungus-feeding bacterial genus Collimonas",
abstract = "Background: Collimonas is a genus belonging to the class of Betaproteobacteria and consists mostly of soil bacteria with the ability to exploit living fungi as food source (mycophagy). Collimonas strains differ in a range of activities, including swimming motility, quorum sensing, extracellular protease activity, siderophore production, and antimicrobial activities. Results: In order to reveal ecological traits possibly related to Collimonas lifestyle and secondary metabolites production, we performed a comparative genomics analysis based on whole-genome sequencing of six strains representing 3 recognized species. The analysis revealed that the core genome represents 43.1 to 52.7 {\%} of the genomes of the six individual strains. These include genes coding for extracellular enzymes (chitinase, peptidase, phospholipase), iron acquisition and type II secretion systems. In the variable genome, differences were found in genes coding for secondary metabolites (e.g. tripropeptin A and volatile terpenes), several unknown orphan polyketide synthase-nonribosomal peptide synthetase (PKS-NRPS), nonribosomal peptide synthetase (NRPS) gene clusters, a new lipopeptide and type III and type VI secretion systems. Potential roles of the latter genes in the interaction with other organisms were investigated. Mutation of a gene involved in tripropeptin A biosynthesis strongly reduced the antibacterial activity against Staphylococcus aureus, while disruption of a gene involved in the biosynthesis of the new lipopeptide had a large effect on the antifungal/oomycetal activities. Conclusions: Overall our results indicated that Collimonas genomes harbour many genes encoding for novel enzymes and secondary metabolites (including terpenes) important for interactions with other organisms and revealed genomic plasticity, which reflect the behaviour, antimicrobial activity and lifestylesof Collimonas spp.",
keywords = "Collimonas, Comparative genomics, Secondary metabolites, Terpenes",
author = "Chunxu Song and Ruth Schmidt and {de Jager}, Victor and Dorota Krzyzanowska and Esmer Jongedijk and Katarina Cankar and Jules Beekwilder and {van Veen}, Anouk and {de Boer}, Wietse and {van Veen}, {Johannes A.} and Paolina Garbeva",
year = "2015",
month = "12",
day = "24",
doi = "10.1186/s12864-015-2289-3",
language = "English",
volume = "16",
journal = "BMC Genomics",
issn = "1471-2164",
publisher = "Springer Verlag",
number = "1",

}

Song, C, Schmidt, R, de Jager, V, Krzyzanowska, D, Jongedijk, E, Cankar, K, Beekwilder, J, van Veen, A, de Boer, W, van Veen, JA & Garbeva, P 2015, 'Exploring the genomic traits of fungus-feeding bacterial genus Collimonas', BMC Genomics, vol. 16, no. 1, 1103. https://doi.org/10.1186/s12864-015-2289-3

Exploring the genomic traits of fungus-feeding bacterial genus Collimonas. / Song, Chunxu; Schmidt, Ruth; de Jager, Victor; Krzyzanowska, Dorota; Jongedijk, Esmer; Cankar, Katarina; Beekwilder, Jules; van Veen, Anouk; de Boer, Wietse; van Veen, Johannes A.; Garbeva, Paolina.

In: BMC Genomics, Vol. 16, No. 1, 1103, 24.12.2015.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Exploring the genomic traits of fungus-feeding bacterial genus Collimonas

AU - Song, Chunxu

AU - Schmidt, Ruth

AU - de Jager, Victor

AU - Krzyzanowska, Dorota

AU - Jongedijk, Esmer

AU - Cankar, Katarina

AU - Beekwilder, Jules

AU - van Veen, Anouk

AU - de Boer, Wietse

AU - van Veen, Johannes A.

AU - Garbeva, Paolina

PY - 2015/12/24

Y1 - 2015/12/24

N2 - Background: Collimonas is a genus belonging to the class of Betaproteobacteria and consists mostly of soil bacteria with the ability to exploit living fungi as food source (mycophagy). Collimonas strains differ in a range of activities, including swimming motility, quorum sensing, extracellular protease activity, siderophore production, and antimicrobial activities. Results: In order to reveal ecological traits possibly related to Collimonas lifestyle and secondary metabolites production, we performed a comparative genomics analysis based on whole-genome sequencing of six strains representing 3 recognized species. The analysis revealed that the core genome represents 43.1 to 52.7 % of the genomes of the six individual strains. These include genes coding for extracellular enzymes (chitinase, peptidase, phospholipase), iron acquisition and type II secretion systems. In the variable genome, differences were found in genes coding for secondary metabolites (e.g. tripropeptin A and volatile terpenes), several unknown orphan polyketide synthase-nonribosomal peptide synthetase (PKS-NRPS), nonribosomal peptide synthetase (NRPS) gene clusters, a new lipopeptide and type III and type VI secretion systems. Potential roles of the latter genes in the interaction with other organisms were investigated. Mutation of a gene involved in tripropeptin A biosynthesis strongly reduced the antibacterial activity against Staphylococcus aureus, while disruption of a gene involved in the biosynthesis of the new lipopeptide had a large effect on the antifungal/oomycetal activities. Conclusions: Overall our results indicated that Collimonas genomes harbour many genes encoding for novel enzymes and secondary metabolites (including terpenes) important for interactions with other organisms and revealed genomic plasticity, which reflect the behaviour, antimicrobial activity and lifestylesof Collimonas spp.

AB - Background: Collimonas is a genus belonging to the class of Betaproteobacteria and consists mostly of soil bacteria with the ability to exploit living fungi as food source (mycophagy). Collimonas strains differ in a range of activities, including swimming motility, quorum sensing, extracellular protease activity, siderophore production, and antimicrobial activities. Results: In order to reveal ecological traits possibly related to Collimonas lifestyle and secondary metabolites production, we performed a comparative genomics analysis based on whole-genome sequencing of six strains representing 3 recognized species. The analysis revealed that the core genome represents 43.1 to 52.7 % of the genomes of the six individual strains. These include genes coding for extracellular enzymes (chitinase, peptidase, phospholipase), iron acquisition and type II secretion systems. In the variable genome, differences were found in genes coding for secondary metabolites (e.g. tripropeptin A and volatile terpenes), several unknown orphan polyketide synthase-nonribosomal peptide synthetase (PKS-NRPS), nonribosomal peptide synthetase (NRPS) gene clusters, a new lipopeptide and type III and type VI secretion systems. Potential roles of the latter genes in the interaction with other organisms were investigated. Mutation of a gene involved in tripropeptin A biosynthesis strongly reduced the antibacterial activity against Staphylococcus aureus, while disruption of a gene involved in the biosynthesis of the new lipopeptide had a large effect on the antifungal/oomycetal activities. Conclusions: Overall our results indicated that Collimonas genomes harbour many genes encoding for novel enzymes and secondary metabolites (including terpenes) important for interactions with other organisms and revealed genomic plasticity, which reflect the behaviour, antimicrobial activity and lifestylesof Collimonas spp.

KW - Collimonas

KW - Comparative genomics

KW - Secondary metabolites

KW - Terpenes

U2 - 10.1186/s12864-015-2289-3

DO - 10.1186/s12864-015-2289-3

M3 - Article

VL - 16

JO - BMC Genomics

T2 - BMC Genomics

JF - BMC Genomics

SN - 1471-2164

IS - 1

M1 - 1103

ER -

Song C, Schmidt R, de Jager V, Krzyzanowska D, Jongedijk E, Cankar K et al. Exploring the genomic traits of fungus-feeding bacterial genus Collimonas. BMC Genomics. 2015 Dec 24;16(1). 1103. https://doi.org/10.1186/s12864-015-2289-3