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A complete enzymatic capacity for biosynthesis of docosahexaenoic acid (DHA, 22 : 6n-3) exists in the marine Harpacticoida copepod Tigriopus californicus.

ABSTRACT: The long-standing paradigm establishing that global production of Omega-3 (n-3) long-chain polyunsaturated fatty acids (LC-PUFA) derived almost exclusively from marine single-cell organisms, was recently challenged by the discovery that multiple invertebrates possess methyl-end (or ωx) desaturases, critical enzymes enabling the biosynthesis of n-3 LC-PUFA. However, the question of whether animals with ωx desaturases have complete n-3 LC-PUFA biosynthetic pathways and hence can contribute to the production of these compounds in marine ecosystems remained unanswered. In the present study, we investigated the complete enzymatic complement involved in the n-3 LC-PUFA biosynthesis in Tigriopus californicus, an intertidal harpacticoid copepod. A total of two ωx desaturases, five front-end desaturases and six fatty acyl elongases were successfully isolated and functionally characterized. The T. californicus ωx desaturases enable the de novo biosynthesis of C₁₈ PUFA such as linoleic and α-linolenic acids, as well as several n-3 LC-PUFA from n-6 substrates. Functions demonstrated in front-end desaturases and fatty acyl elongases unveiled various routes through which T. californicus can biosynthesize the physiologically important arachidonic and eicosapentaenoic acids. Moreover, T. californicus possess a Δ4 desaturase, enabling the biosynthesis of docosahexaenoic acid via the 'Δ4 pathway'. In conclusion, harpacticoid copepods such as T. californicus have complete n-3 LC-PUFA biosynthetic pathways and such capacity illustrates major roles of these invertebrates in the provision of essential fatty acids to upper trophic levels.

SUBMITTER: Kabeya N

PROVIDER: S-EPMC8080000 | biostudies-literature |

REPOSITORIES: biostudies-literature

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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:BACKGROUND:Gene 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. RESULTS:In 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. CONCLUSIONS:The 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.

Dataset Information

A complete enzymatic capacity for biosynthesis of docosahexaenoic acid (DHA, 22 : 6n-3) exists in the marine Harpacticoida copepod Tigriopus californicus.

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