A distinct mitochondrial genome with DUI-like inheritance in the ocean quahog Arctica islandica

Mitochondrial DNA (mtDNA) is strictly maternally inherited in metazoans. The major exception to this rule has been found in many bivalve species which allow the presence of different sex-linked mtDNA molecules. This mechanism, named Doubly Uniparental Inheritance (DUI), is characterized by the presence of 2 mtDNAs: the female mtDNA is found in somatic tissue and female gonads whereas the male mtDNA is usually found in male gonads and sperm. In this study we highlight the existence of two divergent mitochondrial haplotypes with a low genetic difference around 6-8% in Arctica islandica, a long-lived clam belonging to the Arcticidae, a sister group to the Veneridae in which DUI has been found. Phylogenetic analysis on cytochrome b and 16S sequences from somatic and gonadic tissues of clams belonging to different populations reveal the presence of the “divergent” type in male gonads only and the “normal” type in somatic tissues and female gonads. This peculiar segregation of divergent mtDNA types speaks for the occurrence of the DUI mechanism in Arctica islandica. This example also highlights the difficulties to assess the presence of such particular mitochondrial inheritance system and underlines the possible misinterpretations in phylogeographic and phylogenetic studies of bivalve species linked to the presence of two poorly differentiated mitochondrial genomes

Comparative genomic analysis identifies small open reading frames (sORFs) with peptide-encoding features in avian 16S rDNA

International audienc

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

Metazoans normally possess a single lineage of mitochondria inherited from the mother (female-type mitochondria) while paternal mitochondria are absent or eliminated in fertilized eggs. In doubly uniparental inheritance (DUI), which is specific to the bivalve Glade including the ocean quahog, Arctica islandica, male-type mitochondria are retained in male gonads and, in a few species, small proportions of male-type mitochondria co-exist with female-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 male-type mitochondria in somatic tissues of the bivalve A. islandica. Mitochondrial genomes differ by similar to 5.5% at DNA sequence level. Exclusive presence of male-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 male-type mitochondria in somatic tissues, 2) male-type mitochondrial genes are transcribed and 3) individuals with d-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

Functional argument for the existence of an avian nitric oxide synthase in muscle mitochondria: Effect of cold acclimation

International audienceWe report the first evidence of a mitochondrial NO synthase (mtNOS) in bird skeletal muscle. In vitro, mtNOS activity stimulated by L-arginine reduced intermyofibrillar mitochondrial oxygen uptake and ATP synthesis rates, stimulated endogenous H2O2 generation, but had no effect on oxidative phosphorylation efficiency. Arginine-induced effects were fully reversed by L-NAME, a known NOS inhibitor. When ducklings were cold exposed for 4 weeks, muscle mitochondria displayed an increased state 3 respiration, a reduced H2O2 generation but no significant alteration in mtNOS activity. We conclude that mtNOS is expressed in avian skeletal muscle. (C) 2010 Federation of European Biochemical Societies. Published by Elsevier B. V. All rights reserved

Extreme mitochondrial DNA divergence underlies genetic conflict over sex determination

International audienceCytoplasmic male sterility (CMS) is a form of genetic conflict over sex determination that results from differences in modes of inheritance between genomic compartments.1, 2, 3 Indeed, maternally transmitted (usually mitochondrial) genes sometimes enhance their transmission by suppressing the male function in a hermaphroditic organism to the detriment of biparentally inherited nuclear genes. Therefore, these hermaphrodites become functionally female and may coexist with regular hermaphrodites in so-called gynodioecious populations.3 CMS has been known in plants since Darwin’s times4 but is previously unknown in the animal kingdom.5, 6, 7, 8 We relate the first observation of CMS in animals. It occurs in a freshwater snail population, where some individuals appear unable to sire offspring in controlled crosses and show anatomical, physiological, and behavioral characters consistent with a suppression of the male function. Male sterility is associated with a mitochondrial lineage that underwent a spectacular acceleration of DNA substitution rates, affecting the entire mitochondrial genome—this acceleration concerns both synonymous and non-synonymous substitutions and therefore results from increased mitogenome mutation rates. Consequently, mitochondrial haplotype divergence within the population is exceptionally high, matching that observed between snail taxa that diverged 475 million years ago. This result is reminiscent of similar accelerations in mitogenome evolution observed in plant clades where gynodioecy is frequent,9,10 both being consistent with arms-race evolution of genome regions implicated in CMS.11,12 Our study shows that genomic conflicts can trigger independent evolution of similar sex-determination systems in plants and animals and dramatically accelerate molecular evolution

Acute ICV insulin injection does not alter physiological parameters such as food intake, body weight and peripheral blood glucose level.

<p>Bar graphs represent food intake <i>(A)</i> and body weight <i>(B)</i> (mean ± SEM) measured on NaCl ICV injection days (NaCl) and 14 mU insulin ICV injection days (Insulin). The means were not statistically different (paired t-test, p>0.05, ns, n = 18). <i>(C)</i> Bar graphs represent the peripheral blood glucose levels (mean ± SEM) measured from tail blood samples 1 h after ICV NaCl injection (NaCl) and 1 h after ICV insulin injection (Insulin). The means were not statistically different (paired t-test, p>0.05, ns; n = 11).</p

Comparison of the mean (± SEM) respiratory frequency in Hz between satiated NaCl (n = 10) and fasted insulin (n = 10) rats during food odor presentation.

<p>Four 10 sec periods were considered: Pre-odor (−10 sec to 0 sec); Odor presentation (start: 0 sec to 10 sec, middle: 10 sec to 20 sec, end: 20 sec to 30 sec). <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0051227#s3" target="_blank">Results</a> are presented for each experimental condition: in the fasted state after 14 mU insulin ICV injection; in the satiated state after NaCl ICV injection. For the four periods, the means of respiratory frequency observed in two experimental conditions were not statistically different. (Two-way repeated measures ANOVA, p>0.05, ns).</p

Overall course of the behavioral experiments.

<p><i>(A)</i> Olfactory detection experiment. Animals were tested daily in the two-tube experimental device over 16 days (D1–D16). <i>Habituation:</i> On the first 3 days (D1–D3), rats were trained to drink pure water from both tubes (W/W) of the experimental cage. <i>Aversion acquisition:</i> On the following 3 days (D4–D6), rats had access to water odorized with isoamyl-acetate (ISO) diluted at 10⁻⁵ in both tubes (10⁻⁵/10⁻⁵). ISO 10⁻⁵ consumption >0.5 mL was paired with an intraperitoneal injection of LiCl (LiCl IP) to induce a conditioned olfactory aversion (COA) to ISO. <i>Aversion test:</i> On D7, the COA efficiency was tested by giving the animals a choice between water odorized with ISO 10⁻⁵ and pure water (10⁻⁵/W). On Habituation, Aversion acquisition and Aversion test days, animals were trained to receive a daily NaCl ICV injection (NaCl ICV). <i>Olfactory detection test:</i> During the Olfactory detection test period (D8–D11), rats were offered a choice between ISO 10⁻⁹ or ISO 10⁻⁸ and pure water (10⁻⁹/W, 10⁻⁸/W). For a given odorant dilution, the animals were tested on two consecutive days: once 1 h after NaCl ICV injection (D8 and D10) and once 1 h after a 14 mU insulin ICV injection (D9 and D11). <i>Aversion re-test:</i> On D12, the COA stability was assessed by giving the rats the choice between ISO 10⁻⁵ and pure water (10⁻⁵/W). <i>Aversion retention</i>: During the Aversion retention period (D15–D16), three days after the Aversion re-test, rats were offered again the choice between ISO 10⁻⁵ and pure water (10⁻⁵/W) and the animals were tested on two consecutive days: once 1 h after a 14 mU insulin ICV injection (D15) and once after a NaCl ICV injection (D16). (<i>B</i>) Sniffing experiment. Animals were tested daily in a whole-body plethysmograph over 7 days. The rats were first allowed to familiarized with the recording chamber for 4 days (Habituation), D1–D4 without (D1, D2) or with (D3, D4) food odor stimulation. During the sniffing test period (Food odor detection test, D5–D7), the animals were tested either in the fasted state (at 10:00 a.m.), 1 h after 14 mU insulin ICV injection (D5); in the fasted state, 1 h after NaCl ICV injection (D6); in the satiated state, 1 h after NaCl ICV injection (at 4:00 p.m.) (D7).</p