Genome Compositional Organization in Gars Shows More Similarities to Mammals than to Other Ray‐Finned Fish

Abstract

Genomic GC content can vary locally, and GC-rich regions are usually associated with increased DNA thermostability in thermophilic prokaryotes and warm-blooded eukaryotes. Among vertebrates, fish and amphibians appeared to possess a distinctly less heterogeneous AT/GC organization in their genomes, whereas cytogenetically detectable GC heterogeneity has so far only been documented in mammals and birds. The subject of our study is the gar, an ancient "living fossil" of a basal ray-finned fish lineage, known from the Cretaceous period. We carried out cytogenomic analysis in two gar genera (Atractosteus and Lepisosteus) uncovering a GC chromosomal pattern uncharacteristic for fish. Bioinformatic analysis of the spotted gar (Lepisosteus oculatus) confirmed a GC compartmentalization on GC profiles of linkage groups. This indicates a rather mammalian mode of compositional organization on gar chromosomes. Gars are thus the only analyzed extant ray-finned fishes with a GC compartmentalized genome. Since gars are cold-blooded anamniotes, our results contradict the generally accepted hypothesis that the phylogenomic onset of GC compartmentalization occurred near the origin of amniotes. Ecophysiological findings of other authors indicate a metabolic similarity of gars with mammals. We hypothesize that gars might have undergone convergent evolution with the tetrapod lineages leading to mammals on both metabolic and genomic levels. Their metabolic adaptations might have left footprints in their compositional genome evolution, as proposed by the metabolic rate hypothesis. The genome organization described here in gars sheds new light on the compositional genome evolution in vertebrates generally and contributes to better understanding of the complexities of the mechanisms involved in this process.

“Holostei versus Halecostomi” Problem: Insight from Cytogenetics of Ancient Nonteleost Actinopterygian Fish, Bowfin Amia calva

“…Moreover, Symonová et al. () demonstrated that gars and bowfin differ in intrachromosomal organization. The application of cytogenetic approaches and bioinformatics analyses revealed genome AT/GC heterogeneity in spotted gar genome (Symonová et al., ).…”

“…Lepisosteiformes represent higher chromosomal counts than bowfin and teleosts. The tropical gar (2n = 56) and the spotted gar (2n = 58) demonstrates difference in 2n by a fusion/fission event of one chromosome pair Symonová et al (2017). Since gars did not undergo the TGD (Amores et al, 2011), their higher chromosomal counts related to teleost were explained by chromosome fusions in the lineage leading to teleosts after divergence from gar but before the TGD .…”

The Spotted Gar: Genomic Journeys into a Lost World

“…Symonova et al. () performed cytogenomic analyses that revealed a unique GC content compartmentalization in gars compared with other ray‐finned fishes and that curiously resemble similar patterns observed in mammals.…”

Genomic Organization and Physical Mapping of Tandemly Arranged Repetitive DNAs in Sterlet<b> </b>(<b><i>Acipenser ruthenus</i></b>)

“…Moreover, due to the homogeneity in base composition common to genomes of poikilothermic organisms [Medrano et al, 1988], Gbanding in fish chromosomes is not comparable with the distinct patterns produced in mammals [Symonová et al, 2016]. Still, sometimes it is possible to use conventional banding methods for chromosome identification in fish [Gold et al, 1990], as acceptable differentially stained patterns of chromosomes can be obtained [Wiberg, 1983;Symonová et al, 2016]. In these cases, the detailed standardization of a karyotype with unequivocal identification of individual chromosome pairs can be achieved by a combined use of conventional cytogenetic approaches and physical mapping as it was done in mammalian species with high chromosome numbers [Breen, 2008] or in species with complex genomes with different ploidy levels [Trifonov et al, 2015].…”

“…Karyotype standardization is complicated by the high chromosome numbers with the prevalence of small elements in the set. Moreover, due to the homogeneity in base composition common to genomes of poikilothermic organisms [Medrano et al, 1988], Gbanding in fish chromosomes is not comparable with the distinct patterns produced in mammals [Symonová et al, 2016]. Still, sometimes it is possible to use conventional banding methods for chromosome identification in fish [Gold et al, 1990], as acceptable differentially stained patterns of chromosomes can be obtained [Wiberg, 1983;Symonová et al, 2016].…”