Species-Specific Codon Context Rules Unveil Non-Neutrality Effects of Synonymous Mutations

Codon pair usage (codon context) is a species specific gene primary structure feature whose evolutionary and functional roles are poorly understood. The data available show that codon-context has direct impact on both translation accuracy and efficiency, but one does not yet understand how it affects these two translation variables or whether context biases shape gene evolution.Here we study codon-context biases using a set of 72 orthologous highly conserved genes from bacteria, archaea, fungi and high eukaryotes to identify 7 distinct groups of codon context rules. We show that synonymous mutations, i.e., neutral mutations that occur in synonymous codons of codon-pairs, are selected to maintain context biases and that non-synonymous mutations, i.e., non-neutral mutations that alter protein amino acid sequences, are also under selective pressure to preserve codon-context biases.Since in vivo studies provide evidence for a role of codon context on decoding fidelity in E. coli and for decoding efficiency in mammalian cells, our data support the hypothesis that, like codon usage, codon context modulates the evolution of gene primary structure and fine tunes the structure of open reading frames for high genome translational fidelity and efficiency in the 3 domains of life

Coral symbiotic algae calcify ex hospite in partnership with bacteria

Dinoflagellates of the genus Symbiodinium are commonly recognized as invertebrate endosymbionts that are of central importance for the functioning of coral reef ecosystems. However, the endosymbiotic phase within Symbiodinium life history is inherently tied to a more cryptic free-living (ex hospite) phase that remains largely unexplored. Here we show that free-living Symbiodinium spp. in culture commonly form calcifying bacterial–algal communities that produce aragonitic spherulites and encase the dinoflagellates as endolithic cells. This process is driven by Symbiodinium photosynthesis but occurs only in partnership with bacteria. Our findings not only place dinoflagellates on the map of microbial–algal organomineralization processes but also point toward an endolithic phase in the Symbiodinium life history, a phenomenon that may provide new perspectives on the biology and ecology of Symbiodinium spp. and the evolutionary history of the coral– dinoflagellate symbiosis

Consensus Guidelines for Advancing Coral Holobiont Genome and Specimen Voucher Deposition

Coral research is being ushered into the genomic era. To fully capitalize on the potential discoveries from this genomic revolution, the rapidly increasing number of high-quality genomes requires effective pairing with rigorous taxonomic characterizations of specimens and the contextualization of their ecological relevance. However, to date there is no formal framework that genomicists, taxonomists, and coral scientists can collectively use to systematically acquire and link these data. Spurred by the recently announced “Coral symbiosis sensitivity to environmental change hub” under the “Aquatic Symbiosis Genomics Project” - a collaboration between the Wellcome Sanger Institute and the Gordon and Betty Moore Foundation to generate gold-standard genome sequences for coral animal hosts and their associated Symbiodiniaceae microalgae (among the sequencing of many other symbiotic aquatic species) - we outline consensus guidelines to reconcile different types of data. The metaorganism nature of the coral holobiont provides a particular challenge in this context and is a key factor to consider for developing a framework to consolidate genomic, taxonomic, and ecological (meta)data. Ideally, genomic data should be accompanied by taxonomic references, i.e., skeletal vouchers as formal morphological references for corals and strain specimens in the case of microalgal and bacterial symbionts (cultured isolates). However, exhaustive taxonomic characterization of all coral holobiont member species is currently not feasible simply because we do not have a comprehensive understanding of all the organisms that constitute the coral holobiont. Nevertheless, guidelines on minimal, recommended, and ideal-case descriptions for the major coral holobiont constituents (coral animal, Symbiodiniaceae microalgae, and prokaryotes) will undoubtedly help in future referencing and will facilitate comparative studies. We hope that the guidelines outlined here, which we will adhere to as part of the Aquatic Symbiosis Genomics Project sub-hub focused on coral symbioses, will be useful to a broader community and their implementation will facilitate cross- and meta-data comparisons and analyses.CV acknowledges funding from the German Research Foundation (DFG), grants 433042944 and 458901010. Open Access publication fees are covered by an institutional agreement of the University of Konstanz

Building consensus around the assessment and interpretation of Symbiodiniaceae diversity

Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.journal articl

Building consensus around the assessment and interpretation of Symbiodiniaceae diversity

Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships

Population ecology of the dinoflagellate species Lingulodinium Polyedrum in southern California

Marine dinoflagellates are an ecologically important phytoplanktonic group that accounts for two thirds of all known harmful algal bloom (HAB) species. This study explores the population ecology of Lingulodinium polyedrum (F. Stein) J.D. Dodge, a common bloom-forming dinoflagellate species in Southern California. Lingulodinium polyedrum is not considered a HAB species, but functions as one of the main model organisms for dinoflagellate biology. As such, knowledge about this species also contributes significantly to the understanding of dinoflagellate population dynamics at a more general level. In an attempt to understand some of the complex interactions that govern L. polyedrum population ecology, laboratory experiments of life cycle control and intraspecific phenotypic diversity were linked with an in situ study of the population dynamics and the intraspecific genetic diversity of this species in coastal waters of Southern California. The life cycle experiments showed that processes such as gametogenesis and ecdysis of L. polyedrum are influenced by photon flux density (PFD) and gave a first indication for an involvement of the photosynthetic apparatus in the induction of gametogenesis in dinoflagellates. The light acclimation experiments revealed, for the first time, intraspecific phenotypic diversity in L. polyedrum. The two studied strains differed distinctly in their light requirements and light acclimation ‘strategies’. For the study of intraspecific genetic diversity in L. polyedrum a novel method was developed that allowed the genotyping of individual cells. The application of this novel approach to natural populations showed that population genetic exchange of L. polyedrum in the Southern California Bight is tied to water circulation patterns and that both habitat structure and environmental change leave their signatures in the population genetic composition of L. polyedrum. This thesis represents one of the most comprehensive studies of dinoflagellate population ecology and builds the basis for the development of a holistic concept of the population ecology of L. polyedrum and other dinoflagellate species

The Photoprotective Behavior of a Motile Benthic Diatom as Elucidated from the Interplay Between Cell Motility and Physiological Responses to a Light Microgradient Using a Novel Experimental Setup

International audienceIt has long been hypothesized that benthic motile pennate diatoms use phototaxis to optimize photosynthesis and minimize photoinhibitory damage by adjusting their position within vertical light gradients in coastal benthic sediments. However, experimental evidence to test this hypothesis remains inconclusive, mainly due to methodological difficulties in studying cell behavior and photosynthesis over realistic spatial microscale gradients of irradiance and cell position. In this study, a novel experimental approach was developed and used to test the hypothesis of photosynthesis optimization through motility, based on the combination of single-cell in vivo chlorophyll fluorometry and microfluidic chips. The approach allows the concurrent study of behavior and photosynthetic activity of individual cells of the epipelic diatom species Craspedostauros britannicus exposed to a light microgradient of realistic dimensions, simulating the irradiance and distance scales of light microgradients in benthic sediments. Following exposure to light, (i) cells explored their light environment before initiating light-directed motility; (ii) cells used motility to lower their light dose, when exposed to the highest light intensities; and (iii) motility was combined with reversible non-photochemical quenching, to allow cells to avoid photoinhibition. The results of this proof-of-concept study not only strongly support the photoprotective nature of photobehavior in the studied species but also revealed considerable variability in how individual cells reacted to a light microgradient. The experimental setup can be readily applied to study motility and photosynthetic light responses of other diatom species or natural assemblages, as well as other photoautotrophic motile microorganisms, broadening the toolset for experimental microbial ecology research

Symbiodinium-Induced Formation of Microbialites: Mechanistic Insights From in Vitro Experiments and the Prospect of Its Occurrence in Nature

Dinoflagellates in the genus Symbiodinium exhibit a variety of life styles, ranging from mutualistic endosymbioses with animal and protist hosts to free-living life styles. In culture, Symbiodinium spp. and naturally associated bacteria are known to form calcifying biofilms that produce so-called symbiolites, i.e., aragonitic microbialites that incorporate Symbiodinium as endolithic cells. In this study, we investigated (i) how algal growth and the combined physiological activity of these bacterial-algal associations affect the physicochemical macroenvironment in culture and the microenvironment within bacterial-algal biofilms, and (ii) how these interactions induce the formation of symbiolites. In batch culture, calcification typically commenced when Symbiodinium spp. growth approached stationary phase and when photosynthetic activity and its influence on pH and the carbonate system of the culture medium had already subsided, indicating that symbiolite formation is not simply a function of photosynthetic activity in the bulk medium. Physical disturbance of bacteria-algal biofilms, via repeated detaching and dispersing of the developing biofilm, generally impeded symbiolite formation, suggesting that the structural integrity of biofilms plays an important role in generating conditions conducive to calcification. Microsensor measurements of pH and O2 revealed a biofilm microenvironment characterized by high photosynthetic rates and by dynamic changes in photosynthesis and respiration with light intensity and culture age. Ca2+ microsensor measurements confirmed the significance of the biofilm microenvironment in inducing calcification, as photosynthesis within the biofilm induced calcification without the influence of batch culture medium and under environmentally relevant flow conditions. Furthermore, first quantitative data on calcification from 26 calcifying cultures enabled a first broad comparison of Symbiodinium-induced bacterial-algal calcification with other calcification processes. Our findings support the idea that symbiolite formation is a typical, photosynthesis-induced, bacterial-algal calcification process that is likely to occur under natural conditions

Presentation_1_Symbiodinium-Induced Formation of Microbialites: Mechanistic Insights From in Vitro Experiments and the Prospect of Its Occurrence in Nature.pdf

<p>Dinoflagellates in the genus Symbiodinium exhibit a variety of life styles, ranging from mutualistic endosymbioses with animal and protist hosts to free-living life styles. In culture, Symbiodinium spp. and naturally associated bacteria are known to form calcifying biofilms that produce so-called symbiolites, i.e., aragonitic microbialites that incorporate Symbiodinium as endolithic cells. In this study, we investigated (i) how algal growth and the combined physiological activity of these bacterial-algal associations affect the physicochemical macroenvironment in culture and the microenvironment within bacterial-algal biofilms, and (ii) how these interactions induce the formation of symbiolites. In batch culture, calcification typically commenced when Symbiodinium spp. growth approached stationary phase and when photosynthetic activity and its influence on pH and the carbonate system of the culture medium had already subsided, indicating that symbiolite formation is not simply a function of photosynthetic activity in the bulk medium. Physical disturbance of bacteria-algal biofilms, via repeated detaching and dispersing of the developing biofilm, generally impeded symbiolite formation, suggesting that the structural integrity of biofilms plays an important role in generating conditions conducive to calcification. Microsensor measurements of pH and O₂ revealed a biofilm microenvironment characterized by high photosynthetic rates and by dynamic changes in photosynthesis and respiration with light intensity and culture age. Ca²⁺ microsensor measurements confirmed the significance of the biofilm microenvironment in inducing calcification, as photosynthesis within the biofilm induced calcification without the influence of batch culture medium and under environmentally relevant flow conditions. Furthermore, first quantitative data on calcification from 26 calcifying cultures enabled a first broad comparison of Symbiodinium-induced bacterial-algal calcification with other calcification processes. Our findings support the idea that symbiolite formation is a typical, photosynthesis-induced, bacterial-algal calcification process that is likely to occur under natural conditions.</p