Environmental control of marine phytoplankton stoichiometry in the North Atlantic Ocean.

The stoichiometric coupling of carbon to limiting nutrients in marine phytoplankton regulates the magnitude of biological carbon sequestration in the ocean. While clear links between plankton C:N ratios and environmental drivers have been identified, the nature and direction of these links, as well as their underlying physiological and ecological controls, remain uncertain. We show, with a well-constrained mechanistic model of plankton ecophysiology, that while nitrogen availability and temperature emerge as the main drivers of phytoplankton C:N stoichiometry in the North Atlantic, the biological mechanisms involved vary depending on the spatiotemporal scale and region considered. We find that phytoplankton C:N stoichiometry is overall controlled by nitrogen availability below 40° N, predominantly driven by ecoevolutionary shifts in the functional composition of the phytoplankton communities, while phytoplankton stoichiometric plasticity in response to dropping temperatures and increased grazing pressure dominates at higher latitudes. Our findings highlight the potential of "organisms-to-ecosystems" modeling approaches based on mechanistic models of plankton biology accounting for physiology, ecology, and trait evolution to explore and explain complex observational data and ultimately improve the predictions of global ocean models.

Selective constraints on global plankton dispersal.

Marine microbial communities are highly interconnected assemblages of organisms shaped by ecological drift, natural selection, and dispersal. The relative strength of these forces determines how ecosystems respond to environmental gradients, how much diversity is resident in a community or population at any given time, and how populations reorganize and evolve in response to environmental perturbations. In this study, we introduce a globally resolved population-genetic ocean model in order to examine the interplay of dispersal, selection, and adaptive evolution and their effects on community assembly and global biogeography. We find that environmental selection places strong constraints on global dispersal, even in the face of extremely high assumed rates of adaptation. Changing the relative strengths of dispersal, selection, and adaptation has pronounced effects on community assembly in the model and suggests that barriers to dispersal play a key role in the structuring of marine communities, enhancing global biodiversity and the importance of local historical contingencies.

Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus.

The Southern Ocean houses a diverse and productive community of organisms. Unicellular eukaryotic diatoms are the main primary producers in this environment, where photosynthesis is limited by low concentrations of dissolved iron and large seasonal fluctuations in light, temperature and the extent of sea ice. How diatoms have adapted to this extreme environment is largely unknown. Here we present insights into the genome evolution of a cold-adapted diatom from the Southern Ocean, Fragilariopsis cylindrus, based on a comparison with temperate diatoms. We find that approximately 24.7 per cent of the diploid F. cylindrus genome consists of genetic loci with alleles that are highly divergent (15.1 megabases of the total genome size of 61.1 megabases). These divergent alleles were differentially expressed across environmental conditions, including darkness, low iron, freezing, elevated temperature and increased CO2. Alleles with the largest ratio of non-synonymous to synonymous nucleotide substitutions also show the most pronounced condition-dependent expression, suggesting a correlation between diversifying selection and allelic differentiation. Divergent alleles may be involved in adaptation to environmental fluctuations in the Southern Ocean.

Rapid evolution allows coexistence of highly divergent lineages within the same niche.

Marine microbial communities are extremely complex and diverse. The number of locally coexisting species often vastly exceeds the number of identifiable niches, and taxonomic composition often appears decoupled from local environmental conditions. This is contrary to the view that environmental conditions should select for a few locally well-adapted species. Here we use an individual-based eco-evolutionary model to show that virtually unlimited taxonomic diversity can be supported in highly evolving assemblages, even in the absence of niche separation. With a steady stream of heritable changes to phenotype, competitive exclusion may be weakened, allowing sustained coexistence of nearly neutral phenotypes with highly divergent lineages. This behaviour is robust even to abrupt environmental perturbations that might be expected to cause strong selection pressure and an associated loss of diversity. We, therefore, suggest that rapid evolution and individual-level variability are key drivers of species coexistence and maintenance of microbial biodiversity.

Repeat associated mechanisms of genome evolution and function revealed by the Mus caroli and Mus pahari genomes.

Understanding the mechanisms driving lineage-specific evolution in both primates and rodents has been hindered by the lack of sister clades with a similar phylogenetic structure having high-quality genome assemblies. Here, we have created chromosome-level assemblies of the Mus caroli and Mus pahari genomes. Together with the Mus musculus and Rattus norvegicus genomes, this set of rodent genomes is similar in divergence times to the Hominidae (human-chimpanzee-gorilla-orangutan). By comparing the evolutionary dynamics between the Muridae and Hominidae, we identified punctate events of chromosome reshuffling that shaped the ancestral karyotype of Mus musculus and Mus caroli between 3 and 6 million yr ago, but that are absent in the Hominidae. Hominidae show between four- and sevenfold lower rates of nucleotide change and feature turnover in both neutral and functional sequences, suggesting an underlying coherence to the Muridae acceleration. Our system of matched, high-quality genome assemblies revealed how specific classes of repeats can play lineage-specific roles in related species. Recent LINE activity has remodeled protein-coding loci to a greater extent across the Muridae than the Hominidae, with functional consequences at the species level such as reproductive isolation. Furthermore, we charted a Muridae-specific retrotransposon expansion at unprecedented resolution, revealing how a single nucleotide mutation transformed a specific SINE element into an active CTCF binding site carrier specifically in Mus caroli, which resulted in thousands of novel, species-specific CTCF binding sites. Our results show that the comparison of matched phylogenetic sets of genomes will be an increasingly powerful strategy for understanding mammalian biology.

BioStructures.jl: read, write and manipulate macromolecular structures in Julia.

SUMMARY: Robust, flexible and fast software to read, write and manipulate macromolecular structures is a prerequisite for productively doing structural bioinformatics. We present BioStructures.jl, the first dedicated package in the Julia programming language for dealing with macromolecular structures and the Protein Data Bank. BioStructures.jl builds on the lessons learned with similar packages to provide a large feature set, a flexible object representation and high performance. AVAILABILITY AND IMPLEMENTATION: BioStructures.jl is freely available under the MIT license. Source code and documentation are available at https://github.com/BioJulia/BioStructures.jl. BioStructures.jl is compatible with Julia versions 0.6 and later and is system-independent. CONTACT: j.greener@ucl.ac.uk.

High-throughput 3D modelling to dissect the genetic control of leaf elongation in barley (Hordeum vulgare).

To optimize shoot growth and structure of cereals, we need to understand the genetic components controlling initiation and elongation. While measuring total shoot growth at high throughput using 2D imaging has progressed, recovering the 3D shoot structure of small grain cereals at a large scale is still challenging. Here, we present a method for measuring defined individual leaves of cereals, such as wheat and barley, using few images. Plant shoot modelling over time was used to measure the initiation and elongation of leaves in a bi-parental barley mapping population under low and high soil salinity. We detected quantitative trait loci (QTL) related to shoot growth per se, using both simple 2D total shoot measurements and our approach of measuring individual leaves. In addition, we detected QTL specific to leaf elongation and not to total shoot size. Of particular importance was the detection of a QTL on chromosome 3H specific to the early responses of leaf elongation to salt stress, a locus that could not be detected without the computer vision tools developed in this study.

Pathogen enrichment sequencing (PenSeq) enables population genomic studies in oomycetes.

The oomycete pathogens Phytophthora infestans and P. capsici cause significant crop losses world-wide, threatening food security. In each case, pathogenicity factors, called RXLR effectors, contribute to virulence. Some RXLRs are perceived by resistance proteins to trigger host immunity, but our understanding of the demographic processes and adaptive evolution of pathogen virulence remains poor. Here, we describe PenSeq, a highly efficient enrichment sequencing approach for genes encoding pathogenicity determinants which, as shown for the infamous potato blight pathogen Phytophthora infestans, make up < 1% of the entire genome. PenSeq facilitates the characterization of allelic diversity in pathogen effectors, enabling evolutionary and population genomic analyses of Phytophthora species. Furthermore, PenSeq enables the massively parallel identification of presence/absence variations and sequence polymorphisms in key pathogen genes, which is a prerequisite for the efficient deployment of host resistance genes. PenSeq represents a cost-effective alternative to whole-genome sequencing and addresses crucial limitations of current plant pathogen population studies, which are often based on selectively neutral markers and consequently have limited utility in the analysis of adaptive evolution. The approach can be adapted to diverse microbes and pathogens.

Albugo candida race diversity, ploidy and host-associated microbes revealed using DNA sequence capture on diseased plants in the field.

Physiological races of the oomycete Albugo candida are biotrophic pathogens of diverse plant species, primarily the Brassicaceae, and cause infections that suppress host immunity to other pathogens. However, A. candida race diversity and the consequences of host immunosuppression are poorly understood in the field. We report a method that enables sequencing of DNA of plant pathogens and plant-associated microbes directly from field samples (Pathogen Enrichment Sequencing: PenSeq). We apply this method to explore race diversity in A. candida and to detect A. candida-associated microbes in the field (91 A. candida-infected plants). We show with unprecedented resolution that each host plant species supports colonization by one of 17 distinct phylogenetic lineages, each with an unique repertoire of effector candidate alleles. These data reveal the crucial role of sexual and asexual reproduction, polyploidy and host domestication in A. candida specialization on distinct plant species. Our bait design also enabled phylogenetic assignment of DNA sequences from bacteria and fungi from plants in the field. This paper shows that targeted sequencing has a great potential for the study of pathogen populations while they are colonizing their hosts. This method could be applied to other microbes, especially to those that cannot be cultured.

Marine mixotrophy increases trophic transfer efficiency, mean organism size, and vertical carbon flux.

Mixotrophic plankton, which combine the uptake of inorganic resources and the ingestion of living prey, are ubiquitous in marine ecosystems, but their integrated biogeochemical impacts remain unclear. We address this issue by removing the strict distinction between phytoplankton and zooplankton from a global model of the marine plankton food web. This simplification allows the emergence of a realistic trophic network with increased fidelity to empirical estimates of plankton community structure and elemental stoichiometry, relative to a system in which autotrophy and heterotrophy are mutually exclusive. Mixotrophy enhances the transfer of biomass to larger sizes classes further up the food chain, leading to an approximately threefold increase in global mean organism size and an ∼35% increase in sinking carbon flux.

The Implications of Eco-Evolutionary Processes for the Emergence of Marine Plankton Community Biogeography.

Models of community assembly have been used to illustrate how the many functionally diverse species that compose plankton food webs can coexist. However, the evolutionary processes leading to the emergence of plankton food webs and their interplay with migratory processes and spatial heterogeneity are yet to be explored. We study the eco-evolutionary dynamics of a modeled plankton community structured in both size and space and physiologically constrained by empirical data. We demonstrate that a complex yet ecologically and evolutionarily stable size-structured food web can emerge from an initial set of two monomorphic phytoplankton and zooplankton populations. We also show that the coupling of spatial heterogeneity and migration results in the emergence of specific biogeographic patterns: (i) the emergence of a source-sink structure of the plankton metacommunities, (ii) changes in size diversity dependent on migratory intensity and on the scale at which diversity is considered (local vs. global), and (iii) the emergence of eco-evolutionary provinces (i.e., a spatial unit characterized by some level of abiotic heterogeneity but of homogenous size composition due to horizontal movements) at spatial scales that increase with the strength of the migratory processes.

The Size Dependence of Phytoplankton Growth Rates: A Trade-Off between Nutrient Uptake and Metabolism.

Rates of metabolism and population growth are often assumed to decrease universally with increasing organism size. Recent observations have shown, however, that maximum population growth rates among phytoplankton smaller than ∼6 µm in diameter tend to increase with organism size. Here we bring together observations and theory to demonstrate that the observed change in slope is attributable to a trade-off between nutrient uptake and the potential rate of internal metabolism. Specifically, we apply an established model of phytoplankton growth to explore a trade-off between the ability of cells to replenish their internal quota (which increases with size) and their ability to synthesize new biomass (which decreases with size). Contrary to the metabolic theory of ecology, these results demonstrate that rates of resource acquisition (rather than metabolism) provide the primary physiological constraint on the growth rates of some of the smallest and most numerically abundant photosynthetic organisms on Earth.

Physiological and morphological plasticity in response to nitrogen availability of a yeast widely distributed in the open ocean.

Yeasts are prevalent in the open ocean, yet we have limited understanding of their ecophysiological adaptations, including their response to nitrogen availability, which can have a major role in determining the ecological potential of other planktonic microbes. In this study, we characterized the nitrogen uptake capabilities and growth responses of marine-occurring yeasts. Yeast isolates from the North Atlantic Ocean were screened for growth on diverse nitrogen substrates, and across a concentration gradient of three environmentally relevant nitrogen substrates: nitrate, ammonium, and urea. Three strains grew with enriched nitrate while two did not, demonstrating that nitrate utilization is present but not universal in marine yeasts, consistent with existing knowledge of nonmarine yeast strains. Naganishia diffluens MBA_F0213 modified the key functional trait of cell size in response to nitrogen concentration, suggesting yeast cell morphology changes along chemical gradients in the marine environment. Meta-analysis of the reference DNA barcode in public databases revealed that the genus Naganishia has a global ocean distribution, strengthening the environmental applicability of the culture-based observations. This study provides novel quantitative understanding of the ecophysiological and morphological responses of marine-derived yeasts to variable nitrogen availability in vitro, providing insight into the functional ecology of yeasts within pelagic open ocean environments.

The biogeography of marine plankton traits.

Changes in marine plankton communities driven by environmental variability impact the marine food web and global biogeochemical cycles of carbon and other elements. To predict and assess these community shifts and their consequences, ecologists are increasingly investigating how the functional traits of plankton determine their relative fitness along environmental and biological gradients. Laboratory, field and modelling studies are adopting this trait-based approach to map the biogeography of plankton traits that underlies variations in plankton communities. Here, we review progress towards understanding the regulatory roles of several key plankton functional traits, including cell size, N2 -fixation and mixotrophy among phytoplankton, and body size, ontogeny and feeding behaviour for zooplankton. The trait biogeographical approach sheds light on what structures plankton communities in the current ocean, as well as under climate change scenarios, and also allows for finer resolution of community function because community trait composition determines the rates of significant processes, including carbon export. Although understanding of trait biogeography is growing, uncertainties remain that stem, in part, from the paucity of observations describing plankton functional traits. Thus, in addition to recommending widespread adoption of the trait-based approach, we advocate for enhanced collection, standardisation and dissemination of plankton functional trait data.

A multi-objective optimisation model for sewer rehabilitation considering critical risk of failure.

A unique methodology for the optimal specification of sewer rehabilitation investment is presented in this paper. By accounting for the critical risk of asset failure, this methodology builds on previously successful work which explored the application of multi-objective optimisation tools to assist engineers with the specification of optimal rehabilitation strategies. The conventional sewerage rehabilitation specification process relies on the expertise of professional engineers to manually evaluate CCTV inspection information when determining the nature and extent of the rehabilitation solution. This process is not only tedious and subjective but it has no quantifiable means of identifying optimal solutions or possible combinations of optimal solutions in the delivery of catchment wide rehabilitation programmes. Therefore, the purely manual process of sewer rehabilitation design leaves a number of unanswered questions, such as: (1) Does the solution offer the greatest structural benefit to the network? (2) Is the solution the most cost-effective solution available? (3) Does the solution most greatly reduce the risk of critical asset failure? The application of a multi-objective genetic algorithm optimisation model, coupled with an enhanced critical risk methodology, has successfully answered these questions when applied to a case study data set provided by South West Water (UK).

Biophysical aspects of resource acquisition and competition in algal mixotrophs.

Mixotrophic organisms combine autotrophic and heterotrophic nutrition and are abundant in both freshwater and marine environments. Recent observations indicate that mixotrophs constitute a large fraction of the biomass, bacterivory, and primary production in oligotrophic environments. While mixotrophy allows greater flexibility in terms of resource acquisition, any advantage must be traded off against an associated increase in metabolic costs, which appear to make mixotrophs uncompetitive relative to obligate autotrophs and heterotrophs. Using an idealized model of cell physiology and community competition, we identify one mechanism by which mixotrophs can effectively outcompete specialists for nutrient elements. At low resource concentrations, when the uptake of nutrients is limited by diffusion toward the cell, the investment in cell membrane transporters can be minimized. In this situation, mixotrophs can acquire limiting elements in both organic and inorganic forms, outcompeting their specialist competitors that can utilize only one of these forms. This advantage can be enough to offset as much as a twofold increase in additional metabolic costs incurred by mixotrophs. This mechanism is particularly relevant for the maintenance of mixotrophic populations and productivity in the highly oligotrophic subtropical oceans.

The impact of marine nutrient abundance on early eukaryotic ecosystems.

The rise of eukaryotes to ecological prominence represents one of the most dramatic shifts in the history of Earth's biosphere. However, there is an enigmatic temporal lag between the emergence of eukaryotic organisms in the fossil record and their much later ecological expansion. In parallel, there is evidence for a secular increase in the availability of the key macronutrient phosphorus (P) in Earth's oceans. Here, we use an Earth system model equipped with a size-structured marine ecosystem to explore relationships between plankton size, trophic complexity, and the availability of marine nutrients. We find a strong dependence of planktonic ecosystem structure on ocean nutrient abundance, with a larger ocean nutrient inventory leading to greater overall biomass, broader size spectra, and increasing abundance of large Zooplankton. If existing estimates of Proterozoic marine nutrient levels are correct, our results suggest that increases in the ecological impact of eukaryotic algae and trophic complexity in eukaryotic ecosystems were directly linked to restructuring of the global P cycle associated with the protracted rise of surface oxygen levels. Our results thus suggest an indirect but potentially important mechanism by which ocean oxygenation may have acted to shape marine ecological function during late Proterozoic time.

Algal plankton turn to hunting to survive and recover from end-Cretaceous impact darkness.

The end-Cretaceous bolide impact triggered the devastation of marine ecosystems. However, the specific kill mechanism(s) are still debated, and how primary production subsequently recovered remains elusive. We used marine plankton microfossils and eco-evolutionary modeling to determine strategies for survival and recovery, finding that widespread phagotrophy (prey ingestion) was fundamental to plankton surviving the impact and also for the subsequent reestablishment of primary production. Ecological selectivity points to extreme post-impact light inhibition as the principal kill mechanism, with the marine food chain temporarily reset to a bacteria-dominated state. Subsequently, in a sunlit ocean inhabited by only rare survivor grazers but abundant small prey, it was mixotrophic nutrition (autotrophy and heterotrophy) and increasing cell sizes that enabled the eventual reestablishment of marine food webs some 2 million years later.

Neutrophil microvesicles drive atherosclerosis by delivering miR-155 to atheroprone endothelium.

Neutrophils are implicated in the pathogenesis of atherosclerosis but are seldom detected in atherosclerotic plaques. We investigated whether neutrophil-derived microvesicles may influence arterial pathophysiology. Here we report that levels of circulating neutrophil microvesicles are enhanced by exposure to a high fat diet, a known risk factor for atherosclerosis. Neutrophil microvesicles accumulate at disease-prone regions of arteries exposed to disturbed flow patterns, and promote vascular inflammation and atherosclerosis in a murine model. Using cultured endothelial cells exposed to disturbed flow, we demonstrate that neutrophil microvesicles promote inflammatory gene expression by delivering miR-155, enhancing NF-κB activation. Similarly, neutrophil microvesicles increase miR-155 and enhance NF-κB at disease-prone sites of disturbed flow in vivo. Enhancement of atherosclerotic plaque formation and increase in macrophage content by neutrophil microvesicles is dependent on miR-155. We conclude that neutrophils contribute to vascular inflammation and atherogenesis through delivery of microvesicles carrying miR-155 to disease-prone regions.