Dataset Information

Loss of the HIF pathway in a widely distributed intertidal crustacean, the copepod Tigriopus californicus.

ABSTRACT: Hypoxia is a major physiological constraint for which multicellular eukaryotes have evolved robust cellular mechanisms capable of addressing dynamic changes in O2 availability. In animals, oxygen sensing and regulation is primarily performed by the hypoxia-inducible factor (HIF) pathway, and the key components of this pathway are thought to be highly conserved across metazoans. Marine intertidal habitats are dynamic environments, and their inhabitants are known to tolerate wide fluctuations in salinity, temperature, pH, and oxygen. In this study, we show that an abundant intertidal crustacean, the copepod Tigriopus californicus, has lost major genetic components of the HIF pathway, but still shows robust survivorship and transcriptional response to hypoxia. Mining of protein domains across the genome, followed by phylogenetic analyses of gene families, did not identify two key regulatory elements of the metazoan hypoxia response, namely the transcription factor HIF-? and its oxygen-sensing prolyl hydroxylase repressor, EGLN Despite this loss, phenotypic assays revealed that this species is tolerant to extremely low levels of available O2 for at least 24 h at both larval and adult stages. RNA-sequencing (seq) of copepods exposed to nearly anoxic conditions showed differential expression of over 400 genes, with evidence for induction of glycolytic metabolism without a depression of oxidative phosphorylation. Moreover, genes involved in chitin metabolism and cuticle reorganization show categorically a consistent pattern of change during anoxia, highlighting this pathway as a potential solution to low oxygen availability in this small animal with no respiratory structures or pigment.

SUBMITTER: Graham AM

PROVIDER: S-EPMC6600937 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Loss of the HIF pathway in a widely distributed intertidal crustacean, the copepod <i>Tigriopus californicus</i>.

Graham Allie M AM Barreto Felipe S FS

Proceedings of the National Academy of Sciences of the United States of America 20190610 26

Hypoxia is a major physiological constraint for which multicellular eukaryotes have evolved robust cellular mechanisms capable of addressing dynamic changes in O<sub>2</sub> availability. In animals, oxygen sensing and regulation is primarily performed by the hypoxia-inducible factor (HIF) pathway, and the key components of this pathway are thought to be highly conserved across metazoans. Marine intertidal habitats are dynamic environments, and their inhabitants are known to tolerate wide fluctu ...[more]

PMID: 31182611

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Project description:BackgroundAs yet, few genomic resources have been developed in crustaceans. This lack is particularly evident in Copepoda, given the extraordinary numerical abundance, and taxonomic and ecological diversity of this group. Tigriopus californicus is ideally suited to serve as a genetic model copepod and has been the subject of extensive work in environmental stress and reproductive isolation. Accordingly, we set out to develop a broadly-useful panel of genetic markers and to construct a linkage map dense enough for quantitative trait locus detection in an interval mapping framework for T. californicus--a first for copepods.ResultsOne hundred and ninety Single Nucleotide Polymorphisms (SNPs) were used to genotype our mapping population of 250 F2 larvae. We were able to construct a linkage map with an average intermarker distance of 1.8 cM, and a maximum intermarker distance of 10.3 cM. All markers were assembled into linkage groups, and the 12 linkage groups corresponded to the 12 known chromosomes of T. californicus. We estimate a total genome size of 401.0 cM, and a total coverage of 73.7%. Seventy five percent of the mapped markers were detected in 9 additional populations of T. californicus. Of available model arthropod genomes, we were able to show more colocalized pairs of homologues between T. californicus and the honeybee Apis mellifera, than expected by chance, suggesting preserved macrosynteny between Hymenoptera and Copepoda.ConclusionsOur study provides an abundance of linked markers spanning all chromosomes. Many of these markers are also found in multiple populations of T. californicus, and in two other species in the genus. The genomic resource we have developed will enable mapping throughout the geographical range of this species and in closely related species. This linkage map will facilitate genome sequencing, mapping and assembly in an ecologically and taxonomically interesting group for which genomic resources are currently under development.

Project description:BackgroundGene conversion of duplicated genes can slow the divergence of paralogous copies over time but can also result in other interesting evolutionary patterns. Islands of genetic divergence that persist in the face of gene conversion can point to gene regions undergoing selection for new functions. Novel combinations of genetic variation that differ greatly from the original sequence can result from the transfer of genetic variation between paralogous genes by rare gene conversion events. Genetically divergent populations of the copepod Tigriopus californicus provide an excellent model to look at the patterns of divergence among paralogs across multiple independent evolutionary lineages.ResultsIn this study the evolution of a set of paralogous genes encoding putative aspartate transaminase proteins (called GOT1 here) are examined in populations of the copepod T. californicus. One pair of duplicated genes, GOT1p1 and GOT1p2, has regions of high divergence between the copies in the face of apparent on-going gene conversion. The GOT1p2 gene also has unique haplotypes in two populations that appear to have resulted from a transfer of genetic variation via inter-paralog gene conversion. A second pair of duplicated genes GOT1Sr and GOT1Sd also shows evidence of gene conversion, but this gene conversion does not appear to have maintained each as a functional copy in all populations.ConclusionsThe patterns of conservation and sequence divergence across this set of paralogous genes among populations of T. californicus suggest that some interesting evolutionary patterns are occurring at these loci. The results for the GOT1p1/GOT1p2 paralogs illustrate how gene conversion can factor in the creation of a mosaic pattern of regions of high divergence and low divergence. When coupled with rare gene conversion events of divergent regions, this pattern can result in the formation of novel proteins differing substantially from either original protein. The evolutionary patterns across these paralogs show how gene conversion can both constrain and facilitate diversification of genetic sequences.

Project description:BackgroundGeographic variation in the thermal environment impacts a broad range of biochemical and physiological processes and can be a major selective force leading to local population adaptation. In the intertidal copepod Tigriopus californicus, populations along the coast of California show differences in thermal tolerance that are consistent with adaptation, i.e., southern populations withstand thermal stresses that are lethal to northern populations. To understand the genetic basis of these physiological differences, we use an RNA-seq approach to compare genome-wide patterns of gene expression in two populations known to differ in thermal tolerance.ResultsObserved differences in gene expression between the southern (San Diego) and the northern (Santa Cruz) populations included both the number of affected loci as well as the identity of these loci. However, the most pronounced differences concerned the amplitude of up-regulation of genes producing heat shock proteins (Hsps) and genes involved in ubiquitination and proteolysis. Among the hsp genes, orthologous pairs show markedly different thermal responses as the amplitude of hsp response was greatly elevated in the San Diego population, most notably in members of the hsp70 gene family. There was no evidence of accelerated evolution at the sequence level for hsp genes. Among other sets of genes, cuticle genes were up-regulated in SD but down-regulated in SC, and mitochondrial genes were down-regulated in both populations.ConclusionsMarked changes in gene expression were observed in response to acute sub-lethal thermal stress in the copepod T. californicus. Although some qualitative differences were observed between populations, the most pronounced differences involved the magnitude of induction of numerous hsp and ubiquitin genes. These differences in gene expression suggest that evolutionary divergence in the regulatory pathway(s) involved in acute temperature stress may offer at least a partial explanation of population differences in thermal tolerance observed in Tigriopus.

Dataset Information

Loss of the HIF pathway in a widely distributed intertidal crustacean, the copepod Tigriopus californicus.

Publications

Loss of the HIF pathway in a widely distributed intertidal crustacean, the copepod <i>Tigriopus californicus</i>.

Similar Datasets

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