The More, the Merrier? Multiple Myoglobin Genes in Fish Species, Especially in Gray Bichir (Polypterus senegalus) and Reedfish (Erpetoichthys calabaricus)

Abstract

The members of the globin superfamily are a classical model system to investigate gene evolution and their fates as well as the diversity of protein function. One of the best-known globins is myoglobin (Mb), which is mainly expressed in heart muscle and transports oxygen from the sarcolemma to the mitochondria. Most vertebrates harbor a single copy of the myoglobin gene, but some fish species have multiple myoglobin genes. Phylogenetic analyses indicate an independent emergence of multiple myoglobin genes, whereby the origin is mostly the last common ancestor of each order. By analyzing different transcriptome data sets, we found at least 15 multiple myoglobin genes in the polypterid gray bichir (Polypterus senegalus) and reedfish (Erpetoichthys calabaricus). In reedfish the myoglobin genes are expressed in a broad range of tissues but show very different expression values. In contrast, the Mb genes of the gray bichir show a rather scattered expression pattern; only a few Mb genes were found expressed in the analyzed tissues. Both, gray bichir and reedfish possess lungs which enable them to inhabit shallow and swampy waters throughout tropical Africa with frequently fluctuating and low oxygen concentrations. The myoglobin repertoire probably reflects the molecular adaptation to these conditions. The sequence divergence, the substitution rate and the different expression pattern of multiple myoglobin genes in gray bichir and reedfish imply different functions, probably through sub- and neofunctionalization during evolution.

Myoglobin regulates fatty acid trafficking and lipid metabolism in mammary epithelial cells

“…The ectopic occurrence of MB in tissue beyond skeletal/myocardial muscle was first reported in the liver and other organs of hypoxia-tolerant fish models [ 6 – 8 ]. More recently, we and others found that MB is expressed in several cancer cell lines and epithelial tumors [ 9 – 11 ] and in mouse brown adipose tissue [ 12 , 13 ].…”

Myoglobin expression by alternative transcript in different mesenchymal stem cells compartments

“…The ectopic occurrence of Mb isoforms in tissues different from skeletal/myocardial muscle was first reported in the liver and other organs of hypoxia-tolerant fish models [ 27 – 29 ]. More recently, Mb was found to be expressed in several cancer cell lines and epithelial tumors [ 7 , 30 , 31 ] and in mice brown adipose tissue [ 32 , 33 ].…”

Investigating the impact of whole genome duplication on transposable element evolution in ray-finned fishes

“…To assemble a dataset of TE content across major ray-finned fish lineages, we integrated the results of the repeat analysis of the P. bichir genome with other publicly available analyses of transposable elements in ray-finned fishes. For non-teleosts, this captured TE content from two additional polypteriform genomes for E. calabaricus (Helfenrath et al 2021) and P. senegalus (Fujito and Nonaka 2012), Acipenser ruthenus (Du et al 2020) as a representative of Chondrostei, as well as Lepisosteus oculatus (Braasch et al 2016), L. osseus (Mallik et al 2023), and Amia calva (Thompson et al 2021) as representative holosteans. These data were integrated with data from 98 teleost genomes previously analyzed for TE content (Reinar et al 2023), that capture the majority of major teleost lineages including Elopomorpha, Osteoglossomorpha, Otocephala, and a large number of acanthomorph and non-acanthomorph euteleosts.…”

“…Similarly, the sequencing of the Senegal bichir (Polypterus senegalus) leveraged the anatomy of polypterids to provide critical insights into how vertebrates achieved the transition from water to land (Bi et al 2021). In addition, the recently sequenced genome of a second polypterid, Erpetoichthys calabaricus [Reedfish; Assembly (ErpCal1.1; NCBI Annotation Release 100)], has been deployed alongside the P. senegalus genome to provide further insights into other aspects of early vertebrate diversification that include the evolution of keratins (Kimura and Nikaido 2021), olfactory receptors (Zhang et al 2021), and numerous other traits (Helfenrath et al 2021;Mikami et al 2022). However, based on BUSCO scores, the currently sequenced genome of P. senegalus, remains incomplete.…”