New plastids, old proteins: repeated endosymbiotic acquisitions in kareniacean dinoflagellates.

Dinoflagellates are a diverse group of ecologically significant micro-eukaryotes that can serve as a model system for plastid symbiogenesis due to their susceptibility to plastid loss and replacement via serial endosymbiosis. Kareniaceae harbor fucoxanthin-pigmented plastids instead of the ancestral peridinin-pigmented ones and support them with a diverse range of nucleus-encoded plastid-targeted proteins originating from the haptophyte endosymbiont, dinoflagellate host, and/or lateral gene transfers (LGT). Here, we present predicted plastid proteomes from seven distantly related kareniaceans in three genera (Karenia, Karlodinium, and Takayama) and analyze their evolutionary patterns using automated tree building and sorting. We project a relatively limited ( ~ 10%) haptophyte signal pointing towards a shared origin in the family Chrysochromulinaceae. Our data establish significant variations in the functional distributions of these signals, emphasizing the importance of micro-evolutionary processes in shaping the chimeric proteomes. Analysis of plastid genome sequences recontextualizes these results by a striking finding the extant kareniacean plastids are in fact not all of the same origin, as two of the studied species (Karlodinium armiger, Takayama helix) possess plastids from different haptophyte orders than the rest.

Whole-genome scanning reveals environmental selection mechanisms that shape diversity in populations of the epipelagic diatom Chaetoceros.

Diatoms form a diverse and abundant group of photosynthetic protists that are essential players in marine ecosystems. However, the microevolutionary structure of their populations remains poorly understood, particularly in polar regions. Exploring how closely related diatoms adapt to different environments is essential given their short generation times, which may allow rapid adaptations, and their prevalence in marine regions dramatically impacted by climate change, such as the Arctic and Southern Oceans. Here, we address genetic diversity patterns in Chaetoceros, the most abundant diatom genus and one of the most diverse, using 11 metagenome-assembled genomes (MAGs) reconstructed from Tara Oceans metagenomes. Genome-resolved metagenomics on these MAGs confirmed a prevalent distribution of Chaetoceros in the Arctic Ocean with lower dispersal in the Pacific and Southern Oceans as well as in the Mediterranean Sea. Single-nucleotide variants identified within the different MAG populations allowed us to draw a landscape of Chaetoceros genetic diversity and revealed an elevated genetic structure in some Arctic Ocean populations. Gene flow patterns of closely related Chaetoceros populations seemed to correlate with distinct abiotic factors rather than with geographic distance. We found clear positive selection of genes involved in nutrient availability responses, in particular for iron (e.g., ISIP2a, flavodoxin), silicate, and phosphate (e.g., polyamine synthase), that were further supported by analysis of Chaetoceros transcriptomes. Altogether, these results highlight the importance of environmental selection in shaping diatom diversity patterns and provide new insights into their metapopulation genomics through the integration of metagenomic and environmental data.

Hypometabolism to survive the long polar night and subsequent successful return to light in the diatom Fragilariopsis cylindrus.

Diatoms, the main eukaryotic phytoplankton of the polar marine regions, are essential for the maintenance of food chains specific to Arctic and Antarctic ecosystems, and are experiencing major disturbances under current climate change. As such, it is fundamental to understand the physiological mechanisms and associated molecular basis of their endurance during the long polar night. Here, using the polar diatom Fragilariopsis cylindrus, we report an integrative analysis combining transcriptomic, microscopic and biochemical approaches to shed light on the strategies used to survive the polar night. We reveal that in prolonged darkness, diatom cells enter a state of quiescence with reduced metabolic and transcriptional activity, during which no cell division occurs. We propose that minimal energy is provided by respiration and degradation of protein, carbohydrate and lipid stores and that homeostasis is maintained by autophagy in prolonged darkness. We also report internal structural changes that manifest the morphological acclimation of cells to darkness, including the appearance of a large vacuole. Our results further show that immediately following a return to light, diatom cells are able to use photoprotective mechanisms and rapidly resume photosynthesis, demonstrating the remarkable robustness of polar diatoms to prolonged darkness at low temperature.

Evolutionary conservation and metabolic significance of autophagy in algae.

Autophagy is a highly conserved 'self-digesting' mechanism used in eukaryotes to degrade and recycle cellular components by enclosing them in a double membrane compartment and delivering them to lytic organelles (lysosomes or vacuoles). Extensive studies in plants have revealed how autophagy is intricately linked to essential aspects of metabolism and growth, in both normal and stress conditions, including cellular and organelle homeostasis, nutrient recycling, development, responses to biotic and abiotic stresses, senescence and cell death. However, knowledge regarding autophagic processes in other photosynthetic organisms remains limited. In this review, we attempt to summarize the current understanding of autophagy in algae from a metabolic, molecular and evolutionary perspective. We focus on the composition and conservation of the autophagy molecular machinery in eukaryotes and discuss the role of autophagy in metabolic regulation, cellular homeostasis and stress adaptation in algae. This article is part of the theme issue 'The evolution of plant metabolism'.

From nets to networks: tools for deciphering phytoplankton metabolic interactions within communities and their global significance.

Our oceans are populated with a wide diversity of planktonic organisms that form complex dynamic communities at the base of marine trophic networks. Within such communities are phytoplankton, unicellular photosynthetic taxa that provide an estimated half of global primary production and support biogeochemical cycles, along with other essential ecosystem services. One of the major challenges for microbial ecologists has been to try to make sense of this complexity. While phytoplankton distributions can be well explained by abiotic factors such as temperature and nutrient availability, there is increasing evidence that their ecological roles are tightly linked to their metabolic interactions with other plankton members through complex mechanisms (e.g. competition and symbiosis). Therefore, unravelling phytoplankton metabolic interactions is the key for inferring their dependency on, or antagonism with, other taxa and better integrating them into the context of carbon and nutrient fluxes in marine trophic networks. In this review, we attempt to summarize the current knowledge brought by ecophysiology, organismal imaging, in silico predictions and co-occurrence networks using 'omics data, highlighting successful combinations of approaches that may be helpful for future investigations of phytoplankton metabolic interactions within their complex communities.This article is part of the theme issue 'Connected interactions: enriching food web research by spatial and social interactions'.

Presence of vitamin B12 metabolism in the last common ancestor of land plants.

Vitamin B12, also known as cobalamin, is an essential organic cofactor for methionine synthase (METH), and is only synthesized by a subset of bacteria. Plants and fungi have an alternative methionine synthase (METE) that does not need B12 and are typically considered not to utilize it. Some algae facultatively utilize B12 because they encode both METE and METH, while other algae are dependent on B12 as they encode METH only. We performed phylogenomic analyses of METE, METH and 11 further proteins involved in B12 metabolism across more than 1600 plant and algal genomes and transcriptomes (e.g. from OneKp), demonstrating the presence of B12-associated metabolism deep into the streptophytes. METH and five further accessory proteins (MTRR, CblB, CblC, CblD and CblJ) were detected in the hornworts (Anthocerotophyta), and two (CblB and CblJ) were identified in liverworts (Marchantiophyta) in the bryophytes, suggesting a retention of B12-metabolism in the last common land plant ancestor. Our data further show more limited distributions for other B12-related proteins (MCM and RNR-II) and B12 dependency in several algal orders. Finally, considering the collection sites of algae that have lost B12 metabolism, we propose freshwater-to-land transitions and symbiotic associations to have been constraining factors for B12 availability in early plant evolution. This article is part of the theme issue 'The evolution of plant metabolism'.

Genome-scale community modelling reveals conserved metabolic cross-feedings in epipelagic bacterioplankton communities.

Marine microorganisms form complex communities of interacting organisms that influence central ecosystem functions in the ocean such as primary production and nutrient cycling. Identifying the mechanisms controlling their assembly and activities is a major challenge in microbial ecology. Here, we integrated Tara Oceans meta-omics data to predict genome-scale community interactions within prokaryotic assemblages in the euphotic ocean. A global genome-resolved co-activity network revealed a significant number of inter-lineage associations across diverse phylogenetic distances. Identified co-active communities include species displaying smaller genomes but encoding a higher potential for quorum sensing, biofilm formation, and secondary metabolism. Community metabolic modelling reveals a higher potential for interaction within co-active communities and points towards conserved metabolic cross-feedings, in particular of specific amino acids and group B vitamins. Our integrated ecological and metabolic modelling approach suggests that genome streamlining and metabolic auxotrophies may act as joint mechanisms shaping bacterioplankton community assembly in the global ocean surface.

Convergent evolution and horizontal gene transfer in Arctic Ocean microalgae.

Microbial communities in the world ocean are affected strongly by oceanic circulation, creating characteristic marine biomes. The high connectivity of most of the ocean makes it difficult to disentangle selective retention of colonizing genotypes (with traits suited to biome specific conditions) from evolutionary selection, which would act on founder genotypes over time. The Arctic Ocean is exceptional with limited exchange with other oceans and ice covered since the last ice age. To test whether Arctic microalgal lineages evolved apart from algae in the global ocean, we sequenced four lineages of microalgae isolated from Arctic waters and sea ice. Here we show convergent evolution and highlight geographically limited HGT as an ecological adaptive force in the form of PFAM complements and horizontal acquisition of key adaptive genes. Notably, ice-binding proteins were acquired and horizontally transferred among Arctic strains. A comparison with Tara Oceans metagenomes and metatranscriptomes confirmed mostly Arctic distributions of these IBPs. The phylogeny of Arctic-specific genes indicated that these events were independent of bacterial-sourced HGTs in Antarctic Southern Ocean microalgae.

Sharing Vitamin B12 between Bacteria and Microalgae Does Not Systematically Occur: Case Study of the Haptophyte Tisochrysis lutea.

Haptophyte microalgae are key contributors to microbial communities in many environments. It has been proposed recently that members of this group would be virtually all dependent on vitamin B12 (cobalamin), an enzymatic cofactor produced only by some bacteria and archaea. Here, we examined the processes of vitamin B12 acquisition by haptophytes. We tested whether co-cultivating the model species Tisochrysis lutea with B12-producing bacteria in vitamin-deprived conditions would allow the microalga to overcome B12 deprivation. While T. lutea can grow by scavenging vitamin B12 from bacterial extracts, co-culture experiments showed that the algae did not receive B12 from its associated bacteria, despite bacteria/algae ratios supposedly being sufficient to allow enough vitamin production. Since other studies reported mutualistic algae-bacteria interactions for cobalamin, these results question the specificity of such associations. Finally, cultivating T. lutea with a complex bacterial consortium in the absence of the vitamin partially rescued its growth, highlighting the importance of microbial interactions and diversity. This work suggests that direct sharing of vitamin B12 is specific to each species pair and that algae in complex natural communities can acquire it indirectly by other mechanisms (e.g., after bacterial lysis).

Mitotic recombination between homologous chromosomes drives genomic diversity in diatoms.

Diatoms, an evolutionarily successful group of microalgae, display high levels of intraspecific genetic variability in natural populations. However, the contribution of various mechanisms generating such diversity is unknown. Here we estimated the genetic micro-diversity within a natural diatom population and mapped the genomic changes arising within clonally propagated diatom cell cultures. Through quantification of haplotype diversity by next-generation sequencing and amplicon re-sequencing of selected loci, we documented a rapid accumulation of multiple haplotypes accompanied by the appearance of novel protein variants in cell cultures initiated from a single founder cell. Comparison of the genomic changes between mother and daughter cells revealed copy number variation and copy-neutral loss of heterozygosity leading to the fixation of alleles within individual daughter cells. The loss of heterozygosity can be accomplished by recombination between homologous chromosomes. To test this hypothesis, we established an endogenous readout system and estimated that the frequency of interhomolog mitotic recombination was under standard growth conditions 4.2 events per 100 cell divisions. This frequency is increased under environmental stress conditions, including treatment with hydrogen peroxide and cadmium. These data demonstrate that copy number variation and mitotic recombination between homologous chromosomes underlie clonal variability in diatom populations. We discuss the potential adaptive evolutionary benefits of the plastic response in the interhomolog mitotic recombination rate, and we propose that this may have contributed to the ecological success of diatoms.

Environmental vulnerability of the global ocean epipelagic plankton community interactome.

Marine plankton form complex communities of interacting organisms at the base of the food web, which sustain oceanic biogeochemical cycles and help regulate climate. Although global surveys are starting to reveal ecological drivers underlying planktonic community structure and predicted climate change responses, it is unclear how community-scale species interactions will be affected by climate change. Here, we leveraged Tara Oceans sampling to infer a global ocean cross-domain plankton co-occurrence network-the community interactome-and used niche modeling to assess its vulnerabilities to environmental change. Globally, this revealed a plankton interactome self-organized latitudinally into marine biomes (Trades, Westerlies, Polar) and more connected poleward. Integrated niche modeling revealed biome-specific community interactome responses to environmental change and forecasted the most affected lineages for each community. These results provide baseline approaches to assess community structure and organismal interactions under climate scenarios while identifying plausible plankton bioindicators for ocean monitoring of climate change.

How haptophytes microalgae mitigate vitamin B12 limitation.

Vitamin B12 (cobalamin) can control phytoplankton development and community composition, with around half of microalgal species requiring this vitamin for growth. B12 dependency is determined by the absence of cobalamin-independent methionine synthase and is unrelated across lineages. Despite their important role in carbon and sulphur biogeochemistry, little is known about haptophytes utilization of vitamin B12 and their ability to cope with its limitation. Here we report the first evaluation of B12 auxotrophy among this lineage based on molecular data of 19 species from 9 families. We assume that all species encode only a B12-dependent methionine synthase, suggesting ubiquitous B12 auxotrophy in this phylum. We further address the effect of different B12 limitations on the molecular physiology of the model haptophyte Tisochrysis lutea. By coupling growth assays in batch and chemostat to cobalamin quantification and expression analyses, we propose that haptophytes use three strategies to cope with B12 limitation. Haptophytes may assimilate dissolved methionine, finely regulate genes involved in methionine cycle and B12 transport and/or limit B12 transport to the mitochondrion. Taken together, these results provide better understanding of B12 metabolism in haptophytes and represent valuable data for deciphering how B12-producing bacteria shape the structure and dynamics of this important phytoplankton community.