An endosymbiotic bacterium in a plant-parasitic nematode: Member of a new Wolbachia supergroup

Haegeman, Annelies; Vanholme, Bartel; Jacob, Joachim; Vandekerckhove, Tom; Claeys, Myriam; Borgonie, Gaëtan; Gheysen, Godelieve

doi:10.1016/j.ijpara.2009.01.006

Cited by 146 publications

(130 citation statements)

References 41 publications

Supporting

Mentioning

120

Contrasting

Unclassified

Order By: Relevance

“…Such events have been shown in several other animals, including nematodes, probably aided by physical proximity of endosymbionts and germline cells (2). Endosymbionts have been reported in several plant-parasitic nematodes (36)(37)(38), all at the vicinity of gametes or eggs. Although transfers appear more evident for endosymbionts, the presence of plant cell wall degradation genes is less likely in these bacteria.…”

Section: Resultsmentioning

confidence: 85%

Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes

Danchin

Rosso

Vieira

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

302

285

View full text Add to dashboard Cite

Lateral gene transfer from prokaryotes to animals is poorly understood, and the scarce documented examples generally concern genes of uncharacterized role in the receiver organism. In contrast, in plant-parasitic nematodes, several genes, usually not found in animals and similar to bacterial homologs, play essential roles for successful parasitism. Many of these encode plant cell wall-degrading enzymes that constitute an unprecedented arsenal in animals in terms of both abundance and diversity. Here we report that independent lateral gene transfers from different bacteria, followed by gene duplications and early gain of introns, have shaped this repertoire. We also show protein immunolocalization data that suggest additional roles for some of these cell wall-degrading enzymes in the late stages of these parasites' life cycle. Multiple functional acquisitions of exogenous genes that provide selective advantage were probably crucial for the emergence and proficiency of plant parasitism in nematodes.LGT) is the transmission of genes between organisms by mechanisms other than vertical inheritance from an ancestor to an offspring. Although largely documented as an important evolutionary mechanism in prokaryotes (1), LGT in animals that have a separate germline and whose genome is segregated in a nucleus is poorly explored. Although some examples have been described (2-4), most concern transfers from endosymbiotic bacteria, and none provide a clear link between the activity of the transferred gene products and the biology of the host species. Thus, arguments are lacking to support a selective advantage that would have driven fixation of transferred genes at the level of a population or species. By contrast, in plant-parasitic nematodes, a series of genes encoding plant cell wall-degrading or -modifying enzymes, which are usually absent from animals, exhibit similarity to bacteria and may thus originate from LGT. These genes are transcriptionally active, their products have been biochemically characterized, they are secreted in plant tissues, and their inactivation impairs parasitism efficiency (5). The most damaging nematodes to agriculture worldwide belong to the suborder Tylenchina in clade IV that comprises root-knot nematodes and cyst nematodes, the two most-studied lineages (SI Appendix, Fig. S1). These nematodes are able to penetrate and migrate into plant tissue and establish sophisticated parasitic interactions with their hosts. Invasion of the root tissues by nematodes requires degradation of the plant cell wall protective barrier, constituted mainly of cellulose and hemicelluloses as well as pectin and its branched decorations. The first plant cell wall-degrading enzymes from an animal were characterized in cyst nematodes in 1998 (6). Ten years later, analysis of the genome of Meloidogyne incognita, the first genome analysis for a plant-parasitic nematode, revealed that the repertoire of cell wall-degrading enzymes in a single species is diverse and abundant with more than 60 genes covering six different pro...

show abstract

Section: Resultsmentioning

confidence: 85%

Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes

Danchin

Rosso

Vieira

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

302

285

View full text Add to dashboard Cite

show abstract

“…However, it also has a much more restricted prevalence in two families of nematode worms: about 20 species of animal-parasitic Onchocercidae (superfamily Filarioidea; the filariae) (Ferri et al 2011) and at least two species of plant-parasitic Pratylenchidae (Haegeman et al 2009). The most salient characteristic of Wolbachia is its astonishing ability to induce a wide diversity of phenotypes in arthropod hosts, from reproductive manipulations, such as cytoplasmic incompatibility and male-killing, to mutualistic roles, including pathogen protection and enhanced fecundity.…”

mentioning

confidence: 99%

Analysis of gene expression from theWolbachiagenome of a filarial nematode supports both metabolic and defensive roles within the symbiosis

et al. 2012

View full text Add to dashboard Cite

The a-proteobacterium Wolbachia is probably the most prevalent, vertically transmitted symbiont on Earth. In contrast with its wide distribution in arthropods, Wolbachia is restricted to one family of animal-parasitic nematodes, the Onchocercidae. This includes filarial pathogens such as Onchocerca volvulus, the cause of human onchocerciasis, or river blindness. The symbiosis between filariae and Wolbachia is obligate, although the basis of this dependency is not fully understood. Previous studies suggested that Wolbachia may provision metabolites (e.g., haem, riboflavin, and nucleotides) and/or contribute to immune defense. Importantly, Wolbachia is restricted to somatic tissues in adult male worms, whereas females also harbor bacteria in the germline. We sought to characterize the nature of the symbiosis between Wolbachia and O. ochengi, a bovine parasite representing the closest relative of O. volvulus. First, we sequenced the complete genome of Wolbachia strain wOo, which revealed an inability to synthesize riboflavin de novo. Using RNA-seq, we also generated endobacterial transcriptomes from male soma and female germline. In the soma, transcripts for membrane transport and respiration were up-regulated, while the gonad exhibited enrichment for DNA replication and translation. The most abundant Wolbachia proteins, as determined by geLC-MS, included ligands for mammalian Toll-like receptors. Enzymes involved in nucleotide synthesis were dominant among metabolism-related proteins, whereas the haem biosynthetic pathway was poorly represented. We conclude that Wolbachia may have a mitochondrion-like function in the soma, generating ATP for its host. Moreover, the abundance of immunogenic proteins in wOo suggests a role in diverting the immune system toward an ineffective antibacterial response.

show abstract

“…Although the potential physical mechanisms of such proposed gene transfer remain elusive and difficult to definitively confirm, evidence for potential avenues of horizontal gene transfer of genes encoding cell wall-modifying enzymes is emerging. The recent discovery of a Wolbachia endosymbiont in R. similis (Haegeman et al, 2009c) presents such a potential for prokaryotic gene transfer and is supported by evidence from Wolbachia symbionts of other nematode and metazoan species . Caution not to overinterpret the role of HGT in evolution of parasitism is given by the monophyletic nature and apparent ancient eukaryotic origin of GH9 enzymes in a wide spectrum of metazoan taxa (Davison and Blaxter, 2005).…”

Section: ) Concluding Remarksmentioning

confidence: 95%

“…In animal-parasitic nematodes and insects, it was proven that genes derived from their bacterial symbiont Wolbachia are present and transcriptionally active in the genome of the nematode or insect (Dunning-Hotopp et al, 2007). Since a Wolbachia-like symbiont was recently discovered in a phytoparasitic nematode species as well (Haegeman et al, 2009c), ancestors of these symbionts could be the origin of some of the cell wall modifying proteins.…”

Section: ) Evolutionary Aspects Of Cell Wall Modifying Proteins A) Imentioning

confidence: 99%

Degradation of the Plant Cell Wall by Nematodes

Davis

Haegeman

Kikuchi

2011

Genomics and Molecular Genetics of Plant-Nematode Interactions

Self Cite

View full text Add to dashboard Cite

An endosymbiotic bacterium in a plant-parasitic nematode: Member of a new Wolbachia supergroup

Cited by 146 publications

References 41 publications

Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes

Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes

Analysis of gene expression from theWolbachiagenome of a filarial nematode supports both metabolic and defensive roles within the symbiosis

Degradation of the Plant Cell Wall by Nematodes

Contact Info

Product

Resources

About