Diversification and adaptive sequence evolution of Caenorhabditis lysozymes (Nematoda: Rhabditidae)

Abstract

BackgroundLysozymes are important model enzymes in biomedical research with a ubiquitous taxonomic distribution ranging from phages up to plants and animals. Their main function appears to be defence against pathogens, although some of them have also been implicated in digestion. Whereas most organisms have only few lysozyme genes, nematodes of the genus Caenorhabditis possess a surprisingly large repertoire of up to 15 genes.ResultsWe used phylogenetic inference and sequence analysis tools to assess the evolution of lysozymes from three congeneric nematode species, Caenorhabditis elegans, C. briggsae, and C. remanei. Their lysozymes fall into three distinct clades, one belonging to the invertebrate-type and the other two to the protist-type lysozymes. Their diversification is characterised by (i) ancestral gene duplications preceding species separation followed by maintenance of genes, (ii) ancestral duplications followed by gene loss in some of the species, and (iii) recent duplications after divergence of species. Both ancestral and recent gene duplications are associated in several cases with signatures of adaptive sequence evolution, indicating that diversifying selection contributed to lysozyme differentiation. Current data strongly suggests that genetic diversity translates into functional diversity.ConclusionGene duplications are a major source of evolutionary innovation. Our analysis provides an evolutionary framework for understanding the diversification of lysozymes through gene duplication and subsequent differentiation. This information is expected to be of major value in future analysis of lysozyme function and in studies of the dynamics of evolution by gene duplication.

Antimicrobial effectors in the nematode Caenorhabditis elegans : an outgroup to the Arthropoda

“…Ten of the genes are most closely related to the lysozymes found in protists (lys), while the remaining six are of the invertebrate type (ilys) [66]. Within these types, the lysozyme genes most likely arose through repeated duplication events across the phylogeny of the genus Caenorhabditis and show repeated episodes of positive selection [66]. To date, their exact function in C. elegans has not yet been studied at the protein level.…”

“…The nematode C. elegans is unique in that its 16 lysozyme genes fall into two very distinct lysozyme types with an enormous level of sequence divergence within a single species. Ten of the genes are most closely related to the lysozymes found in protists (lys), while the remaining six are of the invertebrate type (ilys) [66]. Within these types, the lysozyme genes most likely arose through repeated duplication events across the phylogeny of the genus Caenorhabditis and show repeated episodes of positive selection [66].…”

“…The gene lys-9 is the only gene which does not show any differential gene expression upon microbe exposure (figure 3b). As this gene is very different in sequence from all remaining C. elegans lysozymes and found at the end of a long branch within the lysozyme phylogeny [66], lys-9 may represent a pseudogene or at least show a function unrelated to that of the other lysozymes. Overall, the observed pattern of differential gene expression for the remaining lysozyme genes suggests that they contribute to both defence and digestion in a microbe-specific form.…”

“…Nevertheless, a likely role in worm immunity was inferred from functional analysis at the gene level, including analysis of knock-out mutants, gene silencing through RNAi, or gene expression analysis in transgenic worms. Most of the genes were shown to be expressed in the intestine, while lys-1 is additionally expressed in neurons, lys-7 in larval muscles and lys-8 in the pharynx (reviewed in [66]). Manipulation of gene activity indicated a role in the interaction with microbes for several lysozyme genes.…”

Lysozyme activity of the salivary gland secretion of the medicinal leech h. verbana, h. medicinalis and h. orientalis

“…Остается только предполагать, что в составе CCЖ могут присутствовать не только лизоцимы типа i-(invertebrate), к которому относится дестабилаза-лизоцим [7], но и лизоцимы других типов. Такая возможность следует, например, из анализа генома эволюционно родственного медицинской пиявке организма клубничной нематоды С. elegance, в составе которого обнаружены гены лизоцимов с-, g-и i-типов [18].…”