6 research outputs found
Extensive gene rearrangements in the mitogenomes of congeneric annelid species and insights on the evolutionary history of the genus Ophryotrocha
Background
Annelids are one the most speciose and ecologically diverse groups of metazoans. Although a significant effort has been recently invested in sequencing genomes of a wide array of metazoans, many orders and families within the phylum Annelida are still represented by a single specimen of a single species. The genus of interstitial annelids Ophryotrocha (Dorvilleidae, Errantia, Annelida) is among these neglected groups, despite its extensive use as model organism in numerous studies on the evolution of life history, physiological and ecological traits. To compensate for the paucity of genomic information in this genus, we here obtained novel complete mitochondrial genomes of six Ophryotrocha species using next generation sequencing. In addition, we investigated the evolution of the reproductive mode in the Ophryotrocha genus using a phylogeny based on two mitochondrial markers (COXI and 16S rDNA) and one nuclear fragment (Histone H3).
Results
Surprisingly, gene order was not conserved among the six Ophryotrocha species investigated, and varied greatly as compared to those found in other annelid species within the class Errantia. The mitogenome phylogeny for the six Ophryotrocha species displayed a separation of gonochoric and hermaphroditic species. However, this separation was not observed in the phylogeny based on the COX1, 16S rDNA, and H3 genes. Parsimony and Bayesian ancestral trait reconstruction indicated that gonochorism was the most parsimonious ancestral reproductive mode in Ophryotrocha spp.
Conclusions
Our results highlight the remarkably high level of gene order variation among congeneric species, even in annelids. This encourages the need for additional mitogenome sequencing of annelid taxa in order to properly understand its mtDNA evolution, high biodiversity and phylogenetic relationships. -- Keywords : Molecular phylogeny ; Dorvilleidae ; Mitogenome ; Next generation sequencing ; Model species ; Reproductive mode
Mitochondrial bioenergetic and genomic flexibilities in birds
Les oiseaux sont des organismes endothermes faisant preuve dâune flexibilitĂ© mĂ©tabolique remarquable en rĂ©ponse aux contraintes Ă©nergĂ©tiques inhĂ©rentes Ă leur mode de vie. Cette flexibilitĂ© est notamment stimulĂ©e lors de transitions nutritionnelles pour adapter leur intensitĂ© mĂ©tabolique selon les ressources Ă©nergĂ©tiques disponibles, est dĂ©terminante pour la survie chez ces animaux. Les mitochondries constituant le principal carrefour mĂ©tabolique, en permettant lâessentiel de la production dâATP cellulaire, sont largement impliquĂ©es dans les modulations observĂ©es au cours dâun jeĂ»ne et lors de la rĂ©alimentation. Le but de cette thĂšse Ă©tait dâĂ©tudier la flexibilitĂ© de la fonction mitochondriale face Ă un jeĂ»ne alimentaire et lors de la rĂ©alimentation chez le canard de Barbarie. Plusieurs aspects allant de la bioĂ©nergĂ©tique, Ă lâorganisation anatomique jusquâĂ la gĂ©nomique et lâĂ©volution des espĂšces ont Ă©tĂ© analysĂ©s pour mieux comprendre les modulations impliquĂ©es et leurs interrelations potentielles pour ajuster le fonctionnement mitochondrial aux contraintes Ă©nergĂ©tiques. Une 1Ăšre Ă©tude a dĂ©crit la cinĂ©tique de lâinstallation dâun hypomĂ©tabolisme musculaire associĂ© Ă lâaugmentation de lâefficacitĂ© bioĂ©nergĂ©tique mitochondriale en rĂ©ponse au jeĂ»ne, avec une acclimatation maximale aprĂšs 3 jours. LâĂ©tude en parallĂšle du remodelage des rĂ©seaux grĂące Ă une double approche par anticorps et microscopie confocale a montrĂ© une flexibilitĂ© bidirectionnelle de lâorganisation des rĂ©seaux de mitochondries musculaires, avec une fusion accrue au tout dĂ©but du jeĂ»ne prĂ©cĂ©dant une fragmentation accrue aprĂšs 4 jours. Une 2Ăšme Ă©tude a montrĂ© lâimplication potentielle de lâactivitĂ© de la monoxyde dâazote synthase (NOS) mitochondriale dans les modulations de la bioĂ©nergĂ©tique mitochondriale induites par le jeĂ»ne alimentaire. LâactivitĂ© de la NOS mitochondriale est accrue par le jeĂ»ne et sa modulation in vitro reproduit de façon rapidement rĂ©versible sur des mitochondries musculaires dâoiseaux nourris les effets induits par le jeĂ»ne alimentaire. Une 3Ăšme Ă©tude a explorĂ© la flexibilitĂ© du gĂ©nome mitochondrial pour dĂ©tecter la prĂ©sence de cadres ouverts de lecture (ORF) codant pour des peptides bioactifs, similaires Ă ceux qui chez les mammifĂšres sont codĂ©s par les gĂšnes 12S et 16S et sont mĂ©taboliquement actifs. Les analyses gĂ©nĂ©tiques ont mis en Ă©vidence chez les oiseaux la prĂ©sence dâORFs incorporĂ©s dans le gĂšne codant pour lâARNr 16S et dont lâĂ©volution molĂ©culaire est similaire Ă celle des gĂšnes mitochondriaux codant pour des sous-unitĂ©s de la chaĂźne respiratoire. Parmi les ORFs dĂ©tectĂ©s, certains correspondent Ă ceux dĂ©crits chez les mammifĂšres (humanine, SHLP6). Une 4Ăšme Ă©tude a montrĂ© que la trĂšs forte conservation chez les mammifĂšres, les oiseaux et les ectothermes terrestres, des ORFs situĂ©s sur le gĂšne 16S ne peut ĂȘtre un artĂ©fact liĂ© Ă une contrainte imposĂ©e par la structure de lâARNr codĂ©, nâĂ©tant pas retrouvĂ©e sur des simulations de sĂ©quences gĂ©nĂ©rĂ©es en tenant compte de la structure secondaire et tertiaire. Chez les 3 groupes de vertĂ©brĂ©s Ă©tudiĂ©s, lâORF codant pour lâhumanine, un peptide identifiĂ© chez lâhomme, a subi au cours de lâĂ©volution une pression de sĂ©lection purifiante maintenant sa composition en acides aminĂ©s. Ce travail souligne la remarquable flexibilitĂ© bioĂ©nergĂ©tique et gĂ©nomique des mitochondries chez les oiseaux qui peut contribuer aux ajustements de lâactivitĂ© Ă©nergĂ©tique lors des transitions nutritionnelles. Les rĂ©sultats obtenus ont ouvert un nouveau champ dâinvestigations sur les nouveaux peptides codĂ©s par le gĂ©nome mitochondrial et dont les rĂŽles biologiques restent Ă explorerBirds are endotherms that exhibit a remarkable metabolic flexibility in response to energetic constraints related to their lifestyles. This flexibility is notably involved during nutritional transitions in order to adjust metabolic intensity to the available energy resources, a prerequisite for survival. Mitochondria, that produce most of cellular ATP production, are involved in the modulations observed during a fast and during refeeding. The aim of this thesis was to investigate the flexibility of mitochondrial functions in response to fasting and refeeding in Muscovy ducks (Cairina moschata). Several aspects, ranging from bioenergetics and anatomical organization to genomics and evolution of species, were analysed to better understand the modulations involved to adjust mitochondrial functioning to energy constraints. A first study described the kinetics of the installation of fasting-induced muscle hypometabolism and the associated improved mitochondrial bioenergetics efficiency and showed that maximum acclimation was reached after 3 days. Mitochondrial networks remodelling, investigated by antibodies (Western blot) and confocal microscopy, showed a bidirectional flexibility with an increased fusion at the beginning of the fast preceding an increased fragmentation observable after 4 days of fasting. A second study suggested the potential involvement of a nitric oxide synthase (NOS) activity detected in mitochondrial fractions in the modulations of mitochondrial bioenergetics induced by fasting. The activity of mitochondrial NOS was found to be increased by fasting and its in vitro modulation mimicked the effects induced by fasting in nourished birds, in a rapid and reversible manner. A third study explored the flexibility of the mitochondrial genome in order to detect the presence of open reading frames (ORF) potentially encoding bioactive peptides similar to those described in mammals and that are encoded by small regions included in the 12S and 16S genes. Our genetic analyses demonstrated the presence of ORFs incorporated into the 16S rRNA coding gene of most avian species. The molecular evolution of these ORFs among bird species was found to be similar to that calculated for all mitochondrial genes coding for subunits of the respiratory chain. Among the detected ORFs, some corresponded to those described in mammals (humanin and SHLP6) but others had never been described. A fourth study showed that the very strong nucleotide conservation of ORFs located in the 16S gene, and observed in mammals, birds and terrestrial ectotherms, was not an artifact linked to a constraint imposed by the structure of the encoded rRNA. Indeed, the strong nucleotide conservation was not found on alignments of sequences generated by simulations of evolution that took into account the secondary and tertiary structures of 16S rRNA. In the 3 groups of vertebrates, the ORF coding humanin, a peptide identified in humans, underwent a specific negative selection pressure in order to maintain its amino-acid composition during evolution. In conclusion, this thesis highlighted the remarkable bioenergetics and genomic flexibilities of mitochondrial function in birds, which could contribute to the metabolic adjustments required during nutritional transitions. Our results have also opened up a new field of investigation concerning the putative peptides encoded by the mitochondrial genome and their biological roles remain to be explore
Comparative genomic analysis identifies small open reading frames (sORFs) with peptide-encoding features in avian 16S rDNA
International audienc
Long-Lived Species of Bivalves Exhibit Low MT-DNA Substitution Rates
International audienceBivalves represent valuable taxonomic group for aging studies given their wide variation in longevity (from 1â2 to >500Â years). It is well known that aging is associated to the maintenance of Reactive Oxygen Species homeostasis and that mitochondria phenotype and genotype dysfunctions accumulation is a hallmark of these processes. Previous studies have shown that mitochondrial DNA mutation rates are linked to lifespan in vertebrate species, but no study has explored this in invertebrates. To this end, we performed a Bayesian Phylogenetic Covariance model of evolution analysis using 12 mitochondrial protein-coding genes of 76 bivalve species. Three life history traits (maximum longevity, generation time and mean temperature tolerance) were tested against 1) synonymous substitution rates (dS), 2) conservative amino acid replacement rates (Kc) and 3) ratios of radical over conservative amino acid replacement rates (Kr/Kc). Our results confirm the already known correlation between longevity and generation time and show, for the first time in an invertebrate class, a significant negative correlation between dS and longevity. This correlation was not as strong when generation time and mean temperature tolerance variations were also considered in our model (marginal correlation), suggesting a confounding effect of these traits on the relationship between longevity and mtDNA substitution rate. By confirming the negative correlation between dS and longevity previously documented in birds and mammals, our results provide support for a general pattern in substitution rates
Threshold effect in the H2O2 production of skeletal muscle mitochondria during fasting and refeeding
International audienceUnder nutritional deprivation, the energetic benefits of reducing mitochondrial metabolism are often associated with enhanced harmful pro-oxidant effects and a subsequent long-term negative impact on cellular integrity. However, the flexibility of mitochondrial functioning under stress has rarely been explored during the transition from basal non-phosphorylating to maximal phosphorylating oxygen consumption. Here, we experimentally tested whether ducklings (Cairina moscnata), fasted for 6 days and subsequently refed for 3 days, exhibited modifications to their mitochondrial fluxes, i.e. oxygen consumption, ATP synthesis, reactive oxygen species generation (ROS) and associated ratios, such as the electron leak (% ROS/O) and the oxidative cost of ATP production (% ROS/ATP). This was carried out at different steady-state rates of oxidative phosphorylation in both pectoralis (glycolytic) and gastrocnemius (oxidative) muscles. Fasting induced a decrease in the rates of oxidative phosphorylation and maximal ROS release. These changes were completely reversed by 3 days of refeeding. Yet, the fundamental finding of the present study was the existence of a clear threshold in ROS release and associated ratios, which remained low until a low level of mitochondrial activity was reached (30-40% of maximal oxidative phosphorylation activity)
Hormetic response triggers multifaceted anti-oxidant strategies in immature king penguins (Aptenodytes patagonicus)
International audienceRepeated deep dives are highly pro-oxidative events for air-breathing aquatic foragers such as penguins. At âŁedging, the transition from a strictly terrestrial to a marine lifestyle may therefore trigger a complex set of anti-oxidant responses to prevent chronic oxidative stress in immature penguins but these pro- cesses are still undeâŁned. By combining in vivo and in vitro approaches with transcriptome analysis, we investigated the adaptive responses of sea-acclimatized (SA) immature king penguins (Aptenodytes pa- tagonicus) compared with pre-âŁedging never-immersed (NI) birds. In vivo, experimental immersion into cold water stimulated a higher thermogenic response in SA penguins than in NI birds, but both groups exhibited hypothermia, a condition favouring oxidative stress. In vitro, the pectoralis muscles of SA birds displayed increased oxidative capacity and mitochondrial protein abundance but unchanged reactive oxygen species (ROS) generation per g tissue because ROS production per mitochondria was reduced. The genes encoding oxidant-generating proteins were down-regulated in SA birds while mRNA abundance and activity of the main antioxidant enzymes were up-regulated. Genes encoding proteins involved in repair mechanisms of oxidized DNA or proteins and in degradation processes were also up-regulated in SA birds. Sea life also increased the degree of fatty acid unsaturation in muscle mitochondrial membranes resulting in higher intrinsic susceptibility to ROS. Oxidative damages to protein or DNA were reduced in SA birds. Repeated experimental immersions of NI penguins in cold-water partially mimicked the effects of acclimatization to marine life, modiâŁed the expression of fewer genes related to oxidative stress but in a similar way as in SA birds and increased oxidative damages to DNA. It is concluded that the multi- faceted plasticity observed after marine life may be crucial to maintain redox homeostasis in active tissues subjected to high pro-oxidative pressure in diving birds. Initial immersions in cold-water may initiate an hormetic response triggering essential changes in the adaptive antioxidant response to marine life