Ocean acidification causes fundamental changes in the cellular metabolism of the Arctic copepod Calanus glacialis as detected by metabolomic analysis

Using a targeted metabolomic approach we investigated the effects of low seawater pH on energy metabolism in two late copepodite stages (CIV and CV) of the keystone Arctic copepod species Calanus glacialis. Exposure to decreasing seawater pH (from 8.0 to 7.0) caused increased ATP, ADP and NAD+ and decreased AMP concentrations in stage CIV, and increased ATP and phospho-L-arginine and decreased AMP concentrations in stage CV. Metabolic pathway enrichment analysis showed enrichment of the TCA cycle and a range of amino acid metabolic pathways in both stages. Concentrations of lactate, malate, fumarate and alpha-ketoglutarate (all involved in the TCA cycle) increased in stage CIV, whereas only alpha-ketoglutarate increased in stage CV. Based on the pattern of concentration changes in glucose, pyruvate, TCA cycle metabolites, and free amino acids, we hypothesise that ocean acidification will lead to a shift in energy production from carbohydrate metabolism in the glycolysis toward amino acid metabolism in the TCA cycle and oxidative phosphorylation in stage CIV. In stage CV, concentrations of most of the analysed free fatty acids increased, suggesting in particular that ocean acidification increases the metabolism of stored wax esters in this stage. Moreover, aminoacyl-tRNA biosynthesis was enriched in both stages indicating increased enzyme production to handle low pH stress

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

Climate warming erodes tropical reef habitat through frequency and intensity of episodic hypoxia

Climate warming threatens marine life by increasing metabolic oxygen demand while decreasing oxygen availability. Tropical species living in warm, low oxygen environments may be most at risk, but their tolerances and exposures to these stressors remain poorly documented. We evaluated habitat restrictions for two brittle star species from Caribbean coral reefs by integrating field observations, laboratory experiments and an ecophysiological model. The absence of one species from the warmest reefs results from vital activity restrictions during episodic low oxygen extremes, even though average conditions are well within physiological tolerance limits. Over the past decade, warmer temperatures have been significantly correlated with a greater frequency and intensity of hypoxic events. Continued warming will progressively exclude hypoxia-tolerant species, even if average oxygen remains constant. A warming-driven increase in frequency or intensity of low oxygen extremes could similarly accelerate habitat loss across other marine ecosystems. -- Keywords : Oxygen ; Aquatic hypoxia ; Hypoxia ; Coral reefs ; Oxygen metabolism ; Ocean temperature ; Echinoderms ; Climate change

Predator traits determine food-web architecture across ecosystems

Predator–prey interactions in natural ecosystems generate complex food webs that have a simple universal body-size architecture where predators are systematically larger than their prey. Food-web theory shows that the highest predator–prey body-mass ratios found in natural food webs may be especially important because they create weak interactions with slow dynamics that stabilize communities against perturbations and maintain ecosystem functioning. Identifying these vital interactions in real communities typically requires arduous identification of interactions in complex food webs. Here, we overcome this obstacle by developing predator-trait models to predict average body-mass ratios based on a database comprising 290 food webs from freshwater, marine and terrestrial ecosystems across all continents. We analysed how species traits constrain body-size architecture by changing the slope of the predator–prey body-mass scaling. Across ecosystems, we found high body-mass ratios for predator groups with specific trait combinations including (1) small vertebrates and (2) large swimming or flying predators. Including the metabolic and movement types of predators increased the accuracy of predicting which species are engaged in high body-mass ratio interactions. We demonstrate that species traits explain striking patterns in the body-size architecture of natural food webs that underpin the stability and functioning of ecosystems, paving the way for community-level management of the most complex natural ecosystems

Quels sont les compartiments biologiques les plus affectés par l'exposition à une température élevée durant l'ontogénie? : une étude de cas sur le vers marin Ophryotrocha labronica

RÉSUMÉ: L'utilisation d'une approche intégrative s'avère particulièrement pertinente pour étudier les mécanismes qui sous-tendent les réponses plastiques des organismes face aux changements de température; cette approche met en évidence la façon dont les compartiments biologiques interagissent et sont finement ajustés de manière à créer une réponse intégrée. L'utilisation d'une telle approche est particulièrement pertinente dans le contexte du réchauffement climatique, puisque les réponses plastiques au niveau des mitochondries et du métabolisme aérobie, pourraient permettre aux espèces de faire face aux effets directs de l'élévation rapide des températures. Cela nécessite néanmoins le développement et l'utilisation d'outils moléculaires et physiologiques qui sont généralement inexistants pour les ectothermes marins, à l'exception de certaines espèces d'intérêt commercial et d'aquaculture, pour lesquelles les outils moléculaires ont été développés récemment. Dans ce contexte, cette étude avait pour objectif de développer et d'utiliser une approche intégrative sur l'annélide marin Ophryotrocha labronica La Greca et Bacci 1962 afin de (1) comprendre l'effet de la température élevée sur les réponses mitochondriales et métaboliques et (2) identifier les conséquences sur la croissance, la survie et la reproduction des organismes, et ce, à travers l'ontogénie des individus. Pour ce faire, les individus ont été exposés expérimentalement, dès leur naissance, à une température contrôle (24 °C, température moyenne enregistrée au pic de densité de la population naturelle) et une température élevée (30 °C, augmentation de 2-3 °C par rapport à la température maximale mesurée dans leur habitat). Chaque jour, du sixième jour d'exposition jusqu'à leur première reproduction, un groupe d'individus était prélevé et congelé afin de mesurer l'effet de la température sur les traits biologiques suivants : expression des gènes mitochondriaux, traits physiologiques mitochondriaux et profils métabolomiques. Les traits d'histoire de vie, soit la taille, la survie ainsi que la fertilité et la fécondité, étaient préalablement mesurés. Nos résultats ont démontré que l'exposition des organismes à la température élevée (30 °C) affecte principalement le profil métabolomique d'O. labronica en modifiant les voies et taux métaboliques, mais n'affecte pas fortement sa croissance, sa survie et sa capacité de se reproduire. Ces résultats confirment qu'O. labronica est en mesure de tolérer la température élevée utilisée dans cette étude. Néanmoins, sachant que les effets néfastes de l'exposition aux températures élevées peuvent s'accumuler dans le temps et que les réponses plastiques peuvent changer avec les générations selon l'environnement expérimenté par les générations précédentes, il serait intéressant d'inclure cette approche intégrative dans les expériences multigénérationnelles. Ces études pourraient contribuer à améliorer notre compréhension des mécanismes impliqués dans la réponse des organismes au réchauffement climatique. -- Mot(s) clé(s) en français : Approche intégrative, Réchauffement climatique, Plasticité phénotypique, Expression génétique, Métabolisme. -- ABSTRACT: The use of an integrative approach is useful to study the mechanisms underpinning organisms' plastic responses to temperature changes; it highlights how different biological compartments interact to create a unique integrated response. This is especially relevant in the context of global warming, as plastic changes at the mitochondrial and metabolic levels, could enable species to face the direct impact of a rapid temperature increase. However, this approach requires molecular and physiological tools, lacking for marine ectotherms. Our study applied an integrative approach on the marine annelid Ophryotrocha labronica La Greca and Bacci 1962 to understand the mitochondrial and metabolic responses to elevated temperature throughout its ontogeny, and the subsequent consequence on organisms' fitness. Hatchlings were exposed to a control (24 °C, average temperature recorded at highest population density) and an elevated temperature (30 °C, +2-3 °C from the maximal temperature recorded in their habitat) until their first reproductive event. Groups were sampled daily to measure the effect of temperature in the following traits of the different biological compartments: mitochondrial gene expression and physiological traits, metabolomics profiles and life-history traits. The elevated temperature affected organisms' metabolomics profiles, principally the metabolic pathways and the metabolic flux, but did not impact individuals' growth, survival and ability to reproduce. This indicates that O. labronica is able to tolerate 30 °C. However, as detrimental effects can accumulate through time and generations, future studies combining an integrative approach with a multigenerational exposure will be necessary to improve our mechanistic understanding of species responses to global warming. -- Mot(s) clé(s) en anglais : Integrative approach, Global Warming, Phenotypic plasticity, Gene expression, Mitochondrial physiology, Metabolism

Seawater carbonate chemistry and reproduction, energy metabolism and fatty acid composition of Ophryotrocha japonica and Ophryotrocha robusta

Trans-generational plasticity (TGP) represents a primary mechanism for guaranteeing species persistence under rapid global changes. To date, no study on TGP responses of marine organisms to global change scenarios in the ocean has been conducted on phylogenetically closely related species, and we thus lack a true appreciation for TGP inter-species variation. Consequently, we examined the tolerance and TGP of life-history and physiological traits in two annelid species within the genus Ophryotrocha: one rare (O. robusta) and one common (O. japonica). Both species were exposed over two generations to ocean acidification (OA) and warming (OW) in isolation and in combination (OAW). Warming scenarios led to a decrease in energy production together with an increase in energy requirements, which was lethal for O. robusta before viable offspring could be produced by the F1. Under OA conditions, O. robusta was able to reach the second generation, despite showing lower survival and reproductive performance when compared to control conditions. This was accompanied by a marked increase in fecundity and egg volume in F2 females, suggesting high capacity for TGP under OA. In contrast, O. japonica thrived under all scenarios across both generations, maintaining its fitness levels via adjusting its metabolomic profile. Overall, the two species investigated show a great deal of difference in their ability to tolerate and respond via TGP to future global changes. We emphasize the potential implications this can have for the determination of extinction risk, and consequently, the conservation of phylogenetically closely related species

Within- and trans-generational responses to combined global changes are highly divergent in two congeneric species of marine annelids

Trans-generational plasticity (TGP) represents a primary mechanism for guaranteeing species persistence under rapid global changes. To date, no study on TGP responses of marine organisms to global change scenarios in the ocean has been conducted on phylogenetically closely related species, and we thus lack a true appreciation for TGP inter-species variation. Consequently, we examined the tolerance and TGP of life-history and physiological traits in two annelid species within the genus Ophryotrocha: one rare (O. robusta) and one common (O. japonica). Both species were exposed over two generations to ocean acidification (OA) and warming (OW) in isolation and in combination (OAW). Warming scenarios led to a decrease in energy production together with an increase in energy requirements, which was lethal for O. robusta before viable offspring could be produced by the F1. Under OA conditions, O. robusta was able to reach the second generation, despite showing lower survival and reproductive performance when compared to control conditions. This was accompanied by a marked increase in fecundity and egg volume in F2 females, suggesting high capacity for TGP under OA. In contrast, O. japonica thrived under all scenarios across both generations, maintaining its fitness levels via adjusting its metabolomic profile. Overall, the two species investigated show a great deal of difference in their ability to tolerate and respond via TGP to future global changes. We emphasize the potential implications this can have for the determination of extinction risk, and consequently, the conservation of phylogenetically closely related species

Supplementary material on within- and trans-generational responses to combined global changes in two congeneric species of marine annelids

The extent of species' geographical distribution can help us define their sensitivity to environmental challenges. Rare species are expected to have narrower tolerance windows and reduced plasticity compared to their common relatives. Assessing rare species' tolerance and plasticity under environmental changes will thus help predicting future changes in the structure and functions of ecosystems. We examined the level of tolerance and transgenerational responses of life-history and physiological traits in a rare (Ophryotrocha robusta) and common (Ophryptrocha japonica) marine polychaete species exposed over two generations to ocean acidification (OA: pH -0.5) and warming (OW: + 4 °C) in isolation and combined (OAW: + 4 °C, pH -0.5). Life history traits (growth, fecundity and eggs volume) were measured on a four months period, after which metabolomics profiles were analysed to highlight molecular pattern (energetic metabolism) linked to life history traits' changes. In the rare species, warming scenarios (OW and OAW) led to a decrease in energy production together with an increase in energy requirements, which were shortly lethal before viable offspring could be produced at the first generation. Under OA conditions, the rare species was able to reach the second generation, despite showing lower survival and reproductive performance when compared to control conditions. This was accompanied by a marked increase in fecundity and eggs volume in F2 females, suggesting higher capacity for transgenerational plasticity. Differently, the common species thrived under all scenarios across both generations, by maintaining fitness levels via adjusting its metabolic profile. Overall, whilst the rare species shows greater capacity to plastically adjust its life history responses after two generations under OA, it is not able to cope with future warming conditions due to lower tolerance to heat. If our results are to apply more broadly, given that rare species are most represented across taxa, and possess key ecological roles, our results support the idea that global changes will lead to an important loss in both specific and functional diversity in marine ecosystems

Metabolomics reprogramming of the northern shrimp exposed to combined ocean change drivers

The dataset contains information on the metabolomics reprogramming of the northern shrimp Pandalus borealis collected from four distinct geographic origins (i.e. St. Lawrence Estuary (SLE) 48° 35' N, 68° 35' W, May 2018 ; Eastern Scotian Shelf (ESS), 45° 23' N, 61° 04' W, February 2019 ; Esquiman Channel (EC), 50° 44' N, 57°29' W, July 2019 ; and Northeast Newfoundland Coast (NNC), 50° 18' N, 54° 16' W, November 2019) and exposed for 30 days under laboratory conditions to different ocean global change scenarios of temperature (2, 6, and 10 °C) and pH (7.75 and 7.40), in isolation and in combination. The dataset contains the concentration of key metabolites linked to the aerobic and anaerobic metabolism, expressed as ng metabolite per mg wet weight. Metabolite extraction, identification and quantification was carried out on shrimp muscle tissue by Les laboratoires Iso-BioKem Inc. in February/March 2021

Seawater carbonate chemistry and cellular metabolism of the Arctic copepod Calanus glacialis

Using a targeted metabolomic approach we investigated the effects of low seawater pH on energy metabolism in two late copepodite stages (CIV and CV) of the keystone Arctic copepod species Calanus glacialis. Exposure to decreasing seawater pH (from 8.0 to 7.0) caused increased ATP, ADP and NAD+ and decreased AMP concentrations in stage CIV, and increased ATP and phospho-L-arginine and decreased AMP concentrations in stage CV. Metabolic pathway enrichment analysis showed enrichment of the TCA cycle and a range of amino acid metabolic pathways in both stages. Concentrations of lactate, malate, fumarate and alpha-ketoglutarate (all involved in the TCA cycle) increased in stage CIV, whereas only alpha-ketoglutarate increased in stage CV. Based on the pattern of concentration changes in glucose, pyruvate, TCA cycle metabolites, and free amino acids, we hypothesise that ocean acidification will lead to a shift in energy production from carbohydrate metabolism in the glycolysis toward amino acid metabolism in the TCA cycle and oxidative phosphorylation in stage CIV. In stage CV, concentrations of most of the analysed free fatty acids increased, suggesting in particular that ocean acidification increases the metabolism of stored wax esters in this stage. Moreover, aminoacyl-tRNA biosynthesis was enriched in both stages indicating increased enzyme production to handle low pH stress