Genetic and functional diversity of the multiple lungfish myoglobins

Lüdemann, Julia; Fago, Angela; Wisniewsky, Michelle; Schneider, Igor; Fabrizius, Andrej; Burmester, Thorsten

doi:10.1111/febs.15094

Cited by 6 publications

(6 citation statements)

References 82 publications

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“…Complete myoglobin coding sequences (465 base pairs including initiation and stop codons) were obtained for 55 eulipotyphlan species (38 moles, 14 shrews, 2 erinacids, and 1 solenodon) using capture-hybridisation, transcriptome sequencing, genome mining, and PCR approaches. Consistent with previous surveys that indicate that myoglobin occurs as a single-copy, orthologous gene in the genomes of mammals and other jawed vertebrates ( Schwarze et al, 2014 ), with rare, lineage-specific gene duplications being restricted to certain aquatic lineages such as some Cyprininae (carp and goldfish; Helbo et al, 2012 ) and Dipnoi (lungfishes; Lüdemann et al, 2020 ), we found no evidence for gene paralogues in any of the species examined, with conceptual translations additionally revealing the expected 153 amino-acid peptides in most cases. However, the translated myoglobin proteins of the Chinese mole shrew, both members of the genus Scaptonyx , and the two desman genera are only 152 amino acids in length.…”

Section: Resultssupporting

confidence: 89%

Myoglobin primary structure reveals multiple convergent transitions to semi-aquatic life in the world's smallest mammalian divers

Eastman

Czolacz

et al. 2021

eLife

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Working memory (WM), the ability to actively hold information in memory over a delay period of seconds, is a fundamental constituent of cognition. Delay-period activity in sensory cortices has been observed in WM tasks, but whether and when the activity plays a functional role for memory maintenance remains unclear. Here, we investigated the causal role of auditory cortex (AC) for memory maintenance in mice performing an auditory WM task. Electrophysiological recordings revealed that AC neurons were active not only during the presentation of the auditory stimulus but also early in the delay period. Furthermore, optogenetic suppression of neural activity in AC during the stimulus epoch and early delay period impaired WM performance, whereas suppression later in the delay period did not. Thus, AC is essential for information encoding and maintenance in auditory WM task, especially during the early delay period.

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Section: Resultssupporting

confidence: 89%

Myoglobin primary structure reveals multiple convergent transitions to semi-aquatic life in the world's smallest mammalian divers

Eastman

Czolacz

et al. 2021

eLife

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“…Interestingly, PseMb5a and PseMb7a show high expression values in gonads similar to the high expression levels of Mb5 in gonads of the west African lungfish and Mb3 in south American lungfish ( Koch et al. 2016 ; Lüdemann, Fago, et al. 2019 ).…”

Section: Discussionsupporting

confidence: 61%

“…In lungfish (Dipnoi) there are up to seven distinct Mb genes with different kinetic properties and tissue-specific expression patterns ( Koch et al. 2016 ; Lüdemann, Fago, et al. 2019 ).…”

Section: Introductionmentioning

confidence: 99%

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

Helfenrath¹,

Sauer²,

Kamga

et al. 2021

Genome Biology and Evolution

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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.

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“…Lungfish harbour up to 7 distinct Mb genes that are differentially expressed in various tissues and it has been shown that the Mbs differ in their abilities to confer tolerance towards hypoxia [ 97 ]. Most recently, additional lungfish species ( Protopterus dolloi, Protopterus aethiopicus and Lepidosiren paradoxa ) were described to display a similar diversity of Mb genes and have orthologous Mb genes [ 98 ]. Functional studies have provided evidence for different O 2 binding and enzymatic properties of lungfish Mbs, reflecting multiple subfunctionalization and neofunctionalization events that occurred early in the evolution of lungfish.…”

Section: Vertebrate Globinsmentioning

confidence: 99%

Lessons from the post-genomic era: Globin diversity beyond oxygen binding and transport

et al. 2020

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Vertebrate hemoglobin (Hb) and myoglobin (Mb) were among the first proteins whose structures and sequences were determined over 50 years ago. In the subsequent pregenomic period, numerous related proteins came to light in plants, invertebrates and bacteria, that shared the myoglobin fold, a signature sequence motif characteristic of a 3-on-3 α-helical sandwich. Concomitantly, eukaryote and bacterial globins with a truncated 2-on-2 α-helical fold were discovered. Genomic information over the last 20 years has dramatically expanded the list of known globins, demonstrating their existence in a limited number of archaeal genomes, a majority of bacterial genomes and an overwhelming majority of eukaryote genomes. In vertebrates, 6 additional globin types were identified, namely neuroglobin (Ngb), cytoglobin (Cygb), globin E (GbE), globin X (GbX), globin Y (GbY) and androglobin (Adgb). Furthermore, functions beyond the familiar oxygen transport and storage have been discovered within the vertebrate globin family, including NO metabolism, peroxidase activity, scavenging of free radicals, and signaling functions. The extension of the knowledge on globin functions suggests that the original roles of bacterial globins must have been enzymatic, involved in defense against NO toxicity, and perhaps also as sensors of O 2 , regulating taxis away or towards high O 2 concentrations. In this review, we aimed to discuss the evolution and remarkable functional diversity of vertebrate globins with particular focus on the variety of non-canonical expression sites of mammalian globins and their according impressive variability of atypical functions.

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Genetic and functional diversity of the multiple lungfish myoglobins

Cited by 6 publications

References 82 publications

Myoglobin primary structure reveals multiple convergent transitions to semi-aquatic life in the world's smallest mammalian divers

Myoglobin primary structure reveals multiple convergent transitions to semi-aquatic life in the world's smallest mammalian divers

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

Lessons from the post-genomic era: Globin diversity beyond oxygen binding and transport

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