Comparative transcriptomics across nematode life cycles reveal gene expression conservation and correlated evolution in adjacent developmental stages

Abstract

10Nematodes are highly abundant animals with diverse habitats and lifestyles. Some are 11 free-living while others parasitize animals or plants, and among the latter, infection abilities 12 change across developmental stages to infect hosts and complete life cycles. Although 13 parasitism has independently arisen multiple times over evolutionary history, common 14 pressures of parasitism-such as adapting to the host environment, evading and subverting 15 the host immune system, and changing environments across life cycles-have led phenotypes 16 and developmental stages among parasites to converge. To determine the relationship 17 between transcriptome evolution and morphological divergences among nematodes, we 18 compared 48 transcriptomes of different developmental stages across eight nematode species. 19The transcriptomes were clustered broadly into embryo, larva, and adult stages, suggesting 20 that gene expression is conserved to some extent across the entire nematode life cycle. Such 21 patterns were partly accounted for by tissue-specific genes-such as those in oocytes and the 22 hypodermis-being expressed at different proportions. Although nematodes typically have 3-23 5 larval stages, the transcriptomes for these stages were found to be highly correlated within 24 each species, suggesting high similarity among larval stages across species. For the 25Caenorhabditis elegans-C. briggsae and Strongyloides stercoralis-S. venezuelensis 26 comparisons, we found that around 50% of genes were expressed at multiple stages, whereas 27 half of their orthologues were also expressed in multiple but different stages. Such frequent 28 changes in expression have resulted in concerted transcriptome evolution across adjacent 29 stages, thus generating species-specific transcriptomes over the course of nematode evolution. 30Our study provides a first insight into the evolution of nematode transcriptomes beyond 31 embryonic development. 32 33

Advancing Strongyloides omics data: bridging the gap with Caenorhabditis elegans

“…In general, much less is known about the genes involved during migration or disseminated infection in the lungs compared with other life cycle stages. The transcriptome varies between the parasitic and free-living larval stages in both S. venezuelensis and S. stercoralis and based on their transcriptome, larval stages appear to be separated by life cycle stage rather than species, despite S. venezuelensis and S. stercoralis infecting different hosts (rats and humans, respectively) [71].…”

“…RNAseq transcriptomics of seven life cycle stages of S. stercoralis [67] was used for comparative analysis of developmental larval forms of Strongyloides and C. elegans, to investigate similarities of molecular regulation of developmental arrest between the C. elegans' dauer larvae and parasitic iL3s [71,72]. Genes encoding components in the cGMP pathway (which controls dauer arrest in C. elegans) were upregulated in Strongyloides iL3s, compared to other larval stages.…”

“…The majority of S. papillosus genes are developmentally regulated with 73% of genes differentially expressed across life cycle stages; 10% of S. papillosus genes were differentially expressed between pFs and flFs, 21% were differentially expressed between free-living males (flM) and flFs and 42-45% were differentially expressed between flF/pF and iL3s. In a comparative transcriptomic analysis, 55% of orthologues from S. venezuelensis and S. stercoralis were assigned to different developmental stages including eggs, larvae and adult stages [71].…”