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Presence of male mitochondria in somatic tissues and their functional importance at the whole animal level in the marine bivalve Arctica islandica.

ABSTRACT: Metazoans normally possess a single lineage of mitochondria inherited from the mother (♀-type mitochondria) while paternal mitochondria are absent or eliminated in fertilized eggs. In doubly uniparental inheritance (DUI), which is specific to the bivalve clade including the ocean quahog, Arctica islandica, ♂-type mitochondria are retained in male gonads and, in a few species, small proportions of ♂-type mitochondria co-exist with ♀-type in somatic tissues. To the best of our knowledge, we report, for the first time in metazoan, the natural occurrence of male and female individuals with exclusively ♂-type mitochondria in somatic tissues of the bivalve A. islandica. Mitochondrial genomes differ by ~5.5% at DNA sequence level. Exclusive presence of ♂-type mitochondria affects mitochondrial complexes partially encoded by mitochondrial genes and leads to a sharp drop in respiratory capacity. Through a combination of whole mitochondrial genome sequencing and molecular assays (gene presence and expression), we demonstrate that 1) 11% of individuals of an Icelandic population appear homoplasmic for ♂-type mitochondria in somatic tissues, 2) ♂-type mitochondrial genes are transcribed and 3) individuals with ♂-type mitochondria in somatic cells lose 30% of their wild-type respiratory capacity. This mitochondrial pattern in A. islandica is a special case of DUI, highlighted in individuals from both sexes with functional consequences at cellular and conceivably whole animal level.

SUBMITTER: Degletagne C

PROVIDER: S-EPMC8452683 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The bivalve Arctica islandica is extremely long lived (>400 years) and can tolerate long periods of hypoxia and anoxia. European populations differ in maximum life spans (MLSP) from 40 years in the Baltic to >400 years around Iceland. Characteristic behavior of A. islandica involves phases of metabolic rate depression (MRD) during which the animals burry into the sediment for several days. During these phases the shell water oxygen concentrations reaches hypoxic to anoxic levels, which possibly support the long life span of some populations. We investigated gene regulation in A. islandica from a long-lived (MLSP 150 years) German Bight population and the short-lived Baltic Sea population, experimentally exposed to different oxygen levels. A new A. islandica transcriptome enabled the identification of genes important during hypoxia/anoxia events and, more generally, gene mining for putative stress response and (anti-) aging genes. Expression changes of a) antioxidant defense: Catalase, Glutathione peroxidase, manganese and copper-zinc Superoxide dismutase; b) oxygen sensing and general stress response: Hypoxia inducible factor alpha, Prolyl hydroxylase and Heat-shock protein 70; and c) anaerobic capacity: Malate dehydrogenase and Octopine dehydrogenase, related transcripts were investigated. Exposed to low oxygen, German Bight individuals suppressed transcription of all investigated genes, whereas Baltic Sea bivalves enhanced gene transcription under anoxic incubation (0 kPa) and, further, decreased these transcription levels again during 6 h of re-oxygenation. Hypoxic and anoxic exposure and subsequent re-oxygenation in Baltic Sea animals did not lead to increased protein oxidation or induction of apoptosis, emphasizing considerable hypoxia/re-oxygenation tolerance in this species. The data suggest that the energy saving effect of MRD may not be an attribute of Baltic Sea A. islandica chronically exposed to high environmental variability (oxygenation, temperature, salinity). Contrary, higher physiological flexibility and stress hardening may predispose these animals to perform a pronounced stress response at the expense of life span.

Project description:Bivalve shells are increasingly used as archives for high-resolution paleoclimate analyses. However, there is still an urgent need for quantitative temperature proxies that work without knowledge of the water chemistry-as is required for δ18O-based paleothermometry-and can better withstand diagenetic overprint. Recently, microstructural properties have been identified as a potential candidate fulfilling these requirements. So far, only few different microstructure categories (nacreous, prismatic and crossed-lamellar) of some short-lived species have been studied in detail, and in all such studies, the size and/or shape of individual biomineral units was found to increase with water temperature. Here, we explore whether the same applies to properties of the crossed-acicular microstructure in the hinge plate of Arctica islandica, the microstructurally most uniform shell portion in this species. In order to focus solely on the effect of temperature on microstructural properties, this study uses bivalves that grew their shells under controlled temperature conditions (1, 3, 6, 9, 12 and 15°C) in the laboratory. With increasing temperature, the size of the largest individual biomineral units and the relative proportion of shell occupied by the crystalline phase increased. The size of the largest pores, a specific microstructural feature of A. islandica, whose potential role in biomineralization is discussed here, increased exponentially with culturing temperature. This study employs scanning electron microscopy in combination with automated image processing software, including an innovative machine learning-based image segmentation method. The new method greatly facilitates the recognition of microstructural entities and enables a faster and more reliable microstructural analysis than previously used techniques. Results of this study establish the new microstructural temperature proxy in the crossed-acicular microstructures of A. islandica and point to an overarching control mechanism of temperature on the micrometer-scale architecture of bivalve shells across species boundaries.

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Presence of male mitochondria in somatic tissues and their functional importance at the whole animal level in the marine bivalve Arctica islandica.

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