Universität zu Köln

KIRANGWA, JOSEPH ORCID: 0000-0002-9393-0500 (2024). Investigating the Evolutionary Diversity of Nematodes from a Genomic Perspective. PhD thesis, Universität zu Köln.

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Abstract

The phylum Nematoda comprises a vast array of species with diverse lifestyles. However, our understanding of the genomic mechanisms underlying nematode diversity remains limited. Through extensive genome comparisons among nematodes and related taxa, this thesis has leveraged the newly sequenced high-quality genomes to investigate the evolutionary plasticity of nematode Hox gene complements and genomic loci arrangements. Hox genes are central to metazoan body plan formation, patterning and evolution, playing a critical role in cell fate decisions early in embryonic development in invertebrates and vertebrates. While the archetypical Hox gene cluster consists of members of nine ortholog groups (HOX1-HOX9), arrayed in close linkage in the order in which they have their anterior-posterior patterning effects, nematode Hox gene sets do not fit this model. The Caenorhabditis elegans Hox gene set is not clustered and contains only six Hox genes from four of the ancestral groups. The pattern observed in C. elegans is not typical of the phylum, and variation in orthologue set presence and absence and in genomic organization has been reported. Recent advances in genome sequencing have resulted in the availability of many novel genome assemblies in Nematoda, especially from taxonomic groups that had not been analyzed previously. I have explored Hox gene complements in high-quality genomes of 80 species from all major Clades of Nematoda to understand the evolution of this key set of body pattern genes and especially to probe the origins of the “dispersed” Hox cluster observed in C. elegans. I found that nematodes can have Hox genes from up to six orthology groups. While nematode Hox “clusters” are often interrupted by unrelated genes, I not only identified species in which the cluster is intact and not dispersed but also Hox gene losses, inversions, and translocations within various nematode lineages. This study emphasizes the diversity of Hox gene evolution within the phylum. DNA methylation influences genome evolution by directly affecting transposon silencing, gene expression, genome stability, and mutation rates. DNA methylation has only been scarcely studied in nematodes. Moreover, its study in newly accessible high-quality nematode genomes remains limited. Here I have investigated the presence of genomic signatures of DNA methylation in two phyla, Nematoda and Nematomorpha. I found variations in the conservation of critical DNA methylation enzymes in Nematoda, revealing the dynamic nature of DNA methylation as an evolving epigenetic mechanism. While certain nematode species like C. elegans lack the DNA methylation system, others exhibit variations of DNA Methyltransferases (DNMTs) similar to mammalian DNMT3 and DNMT1 enzymes which are important enzymes responsible for introducing and maintaining genomic DNA methylation. I found this modification to be widespread in some early-branching nematode lineages, including both animal parasitic and free-living species from Clade I, and absent in others like Clade II Enoplean nematodes. Similarly, limnoterrestrial nematomorphs from the superfamily Gordioidea had a full complement of DNMTs responsible for DNA methylation, whereas marine Nectonema munidae showed its absence. This investigation contributes to the existing body of evidence, emphasizing the presence of DNA methylation as an ancient regulatory mechanism in nematodes. Furthermore, it provides evidence of secondary loss of DNA methylation in model organisms like C. elegans and other nematodes belonging to Clades II, III, IV and V, underscoring the evolutionary dynamics of this regulatory process within the Nematoda. Indeed nematodes are abundant and diverse but also include many parasitic species. Previous molecular phylogenetic studies have revealed parasitism of plants and animals has occurred independently many times in nematode evolution. The recent availability of high-quality nematode genomes has enabled the analysis of genetic data from various nematode species. This data holds the potential to enhance our understanding of genetic signatures associated with parasitic lifestyles. Within nematode parasites, there are also parasitoids, which kill their host to complete their lifecycle. Mermithidae and Nematomorpha are parasitoids sharing commonalities in their lifestyle: immature stages infect arthropod hosts, manipulate hosts to induce water-seeking behavior, and emerge as free-living adults, often killing their host. Some of these species are of great economic importance, being evaluated as biological control agents against mosquito vectors responsible for diseases like malaria, and other insect pests, but with scarce genomic resources currently available. Nematomorpha, despite being closely related to Nematoda, has received insufficient attention in genomic research, leading to gaps in our understanding of their diverse genetic makeup. Therefore, I investigated the genetic features encoded in the genomes of both parasitoid taxa to identify similarities and parallels linked to their ecological lifestyles. I performed a comparative analysis of 12 genomes, comprising parasitoid, parasitic and free-living worms. The investigation revealed genomic signatures in parasitoid species, including expanded gene families enriched in neural transmission modulation, likely linked to the known host manipulation that both mermithids and nematomorphs exert on their hosts. The analysis also uncovered a diverse array of conserved transposable element superfamilies across both lineages. The findings from this study provide valuable insights into the potential genomic adaptations associated with parasitoidism in nematode and nematomorph worms. The identification of expanded gene families and conserved transposable element superfamilies sheds light on the molecular underpinnings of their unique biological traits. Additionally, the core set of orthologs specific to parasitoid worms offers new avenues for understanding the evolution of parasitism within these groups of organisms. This comparative genomics resource serves as a significant asset for the research community, facilitating further investigations into the biology and ecology of parasitoid mermithids and nematomorph worms.

Item Type:	Thesis (PhD thesis)
Translated abstract:	Abstract Language UNSPECIFIED German
Creators:	Creators Email ORCID ORCID Put Code KIRANGWA, JOSEPH jkirangw@uni-koeln.de orcid.org/0000-0002-9393-0500 UNSPECIFIED
URN:	urn:nbn:de:hbz:38-742398
Date:	2024
Place of Publication:	KUPS
Language:	English
Faculty:	Faculty of Mathematics and Natural Sciences
Divisions:	Faculty of Mathematics and Natural Sciences > Department of Biology > Zoologisches Institut
Subjects:	Natural sciences and mathematics Life sciences
Uncontrolled Keywords:	Keywords Language Nematodes English Genomics English Evolution English
Date of oral exam:	5 July 2024
Referee:	Name Academic Title Schiffer, Philipp Dr Roth, Siegfried Prof
Refereed:	Yes
URI:	http://kups.ub.uni-koeln.de/id/eprint/74239