Exploring the genomic traits of fungus-feeding bacterial genus Collimonas

Abstract

BackgroundCollimonas 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.ResultsIn 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.ConclusionsOverall 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-2289-3) contains supplementary material, which is available to authorized users.

Mining into interspecific bacterial interactions

“…gpAD87_25000, gpAD87_13180, bAD24_II11090, bAD24_p01610. Despite the advantages made in the field of genome sequencing and genome annotation a vast percentage of bacterial genome sequences remains with unknown function (Galperin and Koonin, 2004;Song et al, 2015). Independent studies also indicated that such "unknown genes" are differentially expressed during interspecific interactions between bacteria (Garbeva et al, 2011b;Garbeva et al, 2014a).…”

The ecological role of volatile mediated interactions belowground

“…By testing various volatile-mediated interactions between phylogenetically different soil bacteria and protists and comparing those with direct trophic interactions, they demonstrated that specific bacterial volatiles can provide early information about suitable prey. In particular, it was shown that terpenes such as β-Linalool, β-Pinene, Germacrene D-4-ol or δ-Cadinene produced by C. pratensis Ter91 (Song et al 2015b) can stimulate protist activity and motility suggesting that terpenes can be key components in VOCs-mediated communication between protists and bacteria (Schulz-Bohm et al 2017a). Interestingly, soil protists such as Dictyostelium discoideum ) produce volatile terpenes.…”

“…This has revealed that, without physical contact, microorganisms are able to drastically alter plant root system development, plant physiology, hormonal pathways, and biomass production (Ryu et al 2004;Blom et al 2011;Wenke et al 2012;Bailly et al 2014;Bitas et al 2015;Ditengou et al 2015;Piechulla et al 2017). mVOCs can also function as a direct source of nutrients for plants (Meldau et al 2013), induce resistance to pathogens in plants (D'Alessandro et al 2014;Kottb et al 2015;Song et al 2015b;Wintermans et al 2016), affect plant secondary metabolite production (Santoro et al 2011), directly inhibit plant pathogens Garbeva et al 2014b;De Vrieze et al 2015;Kottb et al 2015) and induce soil fungistasis and suppressiveness (Garbeva et al 2011a;Van Agtmaal et al 201). Moreover, one single mVOC can show various functions, such as dimethyl disulfide, which improves plant growth by enhancing the availability of reduced sulfur (Meldau et al 2013).…”

“…They are best known to humans as plants metabolites. However, recent studies revealed that terpenes can be produced by all kingdoms of life including prokaryotes (Takamatsu et al 2011;Yamada et al 2012;Yamada et al 2015;Song et al 2015b;Chen et al 2016). Recently, Yamada et al (2015) described a powerful bioinformatics method based on the use of Hidden Markov Models (HMMs) and Protein Families Database (PFAM) search that has allowed the discovery of terpene synthases of bacterial origin and showed that phylogenetically different bacteria can be a rich source of terpenes.…”

“…Recently, Song et al (2015b) showed that the Collimonas strain (Figure 4.2). These results suggest that terpenes play a key role in VOCs-mediated bacteriaprotist interactions as catalysers of protist activity which is in line with terpene-induced stimulations of nematodes (Rasmann et al 2005).…”