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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.

SUBMITTER: Helfenrath K

PROVIDER: S-EPMC8480196 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Amphibious fishes moving from water to land experience continuous changes in environmental forces. How these subtle changes impact behavioural transitions cannot be resolved by comparisons of aquatic and terrestrial locomotion. For example, aquatic and terrestrial locomotion appear distinct in the actinopterygian fish Polypterus senegalus; however, it is unclear how gradual water level changes influence the transition between these locomotor behaviours. We tested the hypothesis in P. senegalus that swimming and walking are part of an incremental continuum of behaviour and muscle activity across the environmental transition from water to land rather than two discrete behaviours, as proposed by previous literature. We exposed P. senegalus to discrete environments from fully aquatic to fully terrestrial while recording body and pectoral fin kinematics and muscle activity. Anterior axial red muscle effort increases as water depth decreases; however, a typical swimming-like anterior-to-posterior wave of axial red muscle activity is always present, even during terrestrial locomotion, indicating gradual motor control changes. Thus, walking appears to be based on swimming-like axial muscle activity whereas kinematic differences between swimming and walking appear to be due to mechanical constraints. A discrete change in left-right pectoral fin coordination from in-phase to out-of-phase at 0.7 body depths relies on adductor muscle activity with a similar duty factor and adductor muscle effort that increases gradually as water depth decreases. Thus, despite distinct changes in kinematic timing, neuromuscular patterning is similar across the water depth continuum. As the observed, gradual increases in axial muscle effort reflect muscle activity changes between aquatic and terrestrial environments observed in other elongate fishes, a modified, swimming-like axial muscle activity pattern for terrestrial locomotion may be common among elongate amphibious fishes.

Dataset Information

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

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