Genome-wide analyses of chitin synthases identify horizontal gene transfers towards bacteria and allow a robust and unifying classification into fungi

Abstract

BackgroundChitin, the second most abundant biopolymer on earth after cellulose, is found in probably all fungi, many animals (mainly invertebrates), several protists and a few algae, playing an essential role in the development of many of them. This polysaccharide is produced by type 2 glycosyltransferases, called chitin synthases (CHS). There are several contradictory classifications of CHS isoenzymes and, as regards their evolutionary history, their origin and diversity is still a matter of debate.ResultsA genome-wide analysis resulted in the detection of more than eight hundred putative chitin synthases in proteomes associated with about 130 genomes. Phylogenetic analyses were performed with special care to avoid any pitfalls associated with the peculiarities of these sequences (e.g. highly variable regions, truncated or recombined sequences, long-branch attraction). This allowed us to revise and unify the fungal CHS classification and to study the evolutionary history of the CHS multigenic family. This update has the advantage of being user-friendly due to the development of a dedicated website (http://wwwabi.snv.jussieu.fr/public/CHSdb), and it includes any correspondences with previously published classifications and mutants. Concerning the evolutionary history of CHS, this family has mainly evolved via duplications and losses. However, it is likely that several horizontal gene transfers (HGT) also occurred in eukaryotic microorganisms and, even more surprisingly, in bacteria.ConclusionsThis comprehensive multi-species analysis contributes to the classification of fungal CHS, in particular by optimizing its robustness, consensuality and accessibility. It also highlights the importance of HGT in the evolutionary history of CHS and describes bacterial chs genes for the first time. Many of the bacteria that have acquired a chitin synthase are plant pathogens (e.g. Dickeya spp; Pectobacterium spp; Brenneria spp; Agrobacterium vitis and Pseudomonas cichorii). Whether they are able to produce a chitin exopolysaccharide or secrete chitooligosaccharides requires further investigation.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0815-9) contains supplementary material, which is available to authorized users.

Genome and evolution of the arbuscular mycorrhizal fungus Diversispora epigaea (formerly Glomus versiforme) and its bacterial endosymbionts

“…The chitin synthase is a type 2 glycosyltransferase involved in the biosynthesis of chitin, a component of the fungal cell wall. Horizontal transfer of chitin synthase genes to bacteria has been reported (Gonçalves et al ., ), and we show that HGT also occurs between the early diverging fungi and endobacteria (Fig. b).…”

Comparative characterization of putative chitin deacetylases from Phaeodactylum tricornutum and Thalassiosira pseudonana highlights the potential for distinct chitin‐based metabolic processes in diatoms

“…On the other hand, CDA from centric diatoms displays a closer genetic relationship with fungi and amoeba, suggesting the probable existence of HGT from Opisthokonta. This was in accordance with the CHS sequences from T. pseudonana , which derived from a single sequence horizontally transferred to the diatom ancestor from a fungus (Gonçalves et al ., ; Morozov & Likhoshway, ). The nesting of Opisthokonta lineage and centric diatom lineage might be further evidence of the eukaryote to eukaryote lateral gene transfer (i.e.…”

Chitinases as Antibacterial Proteins: A Systematic Review

“…23 Unlike fungi, bacteria cell walls do not contain chitin. Although genes encoding chitin synthase (CHS; EC 2.4.1.16), which catalyzes the elongation of chitin, have been recently discovered in some bacterial genomes, 24 species containing CHS genes represent only 0.9% of the 1218 bacterial genomes analyzed and to date there is no experimental evidence that chitin occurs in these few species. This is probably the main reason why many researchers have neglected bacterial species as possible targets for the action of chitinases.…”