Facultative lifestyle drives diversity of coral algal symbionts.

The photosynthetic symbionts of corals sustain biodiverse reefs in nutrient-poor, tropical waters. Recent genomic data illuminate the evolution of coral symbionts under genome size constraints and suggest that retention of the facultative lifestyle, widespread among these algae, confers a selective advantage when compared with a strict symbiotic existence. We posit that the coral symbiosis is analogous to a 'bioreactor' that selects winner genotypes and allows them to rise to high numbers in a sheltered habitat prior to release by the coral host. Our observations lead to a novel hypothesis, the 'stepping-stone model', which predicts that local adaptation under both the symbiotic and free-living stages, in a stepwise fashion, accelerates coral alga diversity and the origin of endemic strains and species.

Endosymbiotic ratchet accelerates divergence after organelle origin: The Paulinella model for plastid evolution: The Paulinella model for plastid evolution.

We hypothesize that as one of the most consequential events in evolution, primary endosymbiosis accelerates lineage divergence, a process we refer to as the endosymbiotic ratchet. Our proposal is supported by recent work on the photosynthetic amoeba, Paulinella, that underwent primary plastid endosymbiosis about 124 Mya. This amoeba model allows us to explore the early impacts of photosynthetic organelle (plastid) origin on the host lineage. The current data point to a central role for effective population size (Ne ) in accelerating divergence post-endosymbiosis due to limits to dispersal and reproductive isolation that reduce Ne , leading to local adaptation. We posit that isolated populations exploit different strategies and behaviors and assort themselves in non-overlapping niches to minimize competition during the early, rapid evolutionary phase of organelle integration. The endosymbiotic ratchet provides a general framework for interpreting post-endosymbiosis lineage evolution that is driven by disruptive selection and demographic and population shifts. Also see the video abstract here: https://youtu.be/gYXrFM6Zz6Q.

Multiple waves of viral invasions in Symbiodiniaceae algal genomes.

Dinoflagellates from the family Symbiodiniaceae are phototrophic marine protists that engage in symbiosis with diverse hosts. Their large and distinct genomes are characterized by pervasive gene duplication and large-scale retroposition events. However, little is known about the role and scale of horizontal gene transfer (HGT) in the evolution of this algal family. In other dinoflagellates, high levels of HGTs have been observed, linked to major genomic transitions, such as the appearance of a viral-acquired nucleoprotein that originated via HGT from a large DNA algal virus. Previous work showed that Symbiodiniaceae from different hosts are actively infected by viral groups, such as giant DNA viruses and ssRNA viruses, that may play an important role in coral health. Latent viral infections may also occur, whereby viruses could persist in the cytoplasm or integrate into the host genome as a provirus. This hypothesis received experimental support; however, the cellular localization of putative latent viruses and their taxonomic affiliation are still unknown. In addition, despite the finding of viral sequences in some genomes of Symbiodiniaceae, viral origin, taxonomic breadth, and metabolic potential have not been explored. To address these questions, we searched for putative viral-derived proteins in thirteen Symbiodiniaceae genomes. We found fifty-nine candidate viral-derived HGTs that gave rise to twelve phylogenies across ten genomes. We also describe the taxonomic affiliation of these virus-related sequences, their structure, and their genomic context. These results lead us to propose a model to explain the origin and fate of Symbiodiniaceae viral acquisitions.

Long-Term Stability of Bacterial Associations in a Microcosm of Ostreococcus tauri (Chlorophyta, Mamiellophyceae).

Phytoplankton-bacteria interactions rule over carbon fixation in the sunlit ocean, yet only a handful of phytoplanktonic-bacteria interactions have been experimentally characterized. In this study, we investigated the effect of three bacterial strains isolated from a long-term microcosm experiment with one Ostreococcus strain (Chlorophyta, Mamiellophyceae). We provided evidence that two Roseovarius strains (Alphaproteobacteria) had a beneficial effect on the long-term survival of the microalgae whereas one Winogradskyella strain (Flavobacteriia) led to the collapse of the microalga culture. Co-cultivation of the beneficial and the antagonistic strains also led to the loss of the microalga cells. Metagenomic analysis of the microcosm is consistent with vitamin B12 synthesis by the Roseovarius strains and unveiled two additional species affiliated to Balneola (Balneolia) and Muricauda (Flavobacteriia), which represent less than 4% of the reads, whereas Roseovarius and Winogradskyella recruit 57 and 39% of the reads, respectively. These results suggest that the low-frequency bacterial species may antagonize the algicidal effect of Winogradskyella in the microbiome of Ostreococcus tauri and thus stabilize the microalga persistence in the microcosm. Altogether, these results open novel perspectives into long-term stability of phytoplankton cultures.

Pervasive transmission of E484K and emergence of VUI-NP13L with evidence of SARS-CoV-2 co-infection events by two different lineages in Rio Grande do Sul, Brazil.

Emergence of novel SARS-CoV-2 lineages are under the spotlight of the media, scientific community and governments. Recent reports of novel variants in the United Kingdom, South Africa and Brazil (B.1.1.28-E484K) have raised intense interest because of a possible higher transmission rate or resistance to the novel vaccines. Nevertheless, the spread of B.1.1.28 (E484K) and other variants in Brazil is still unknown. In this work, we investigated the population structure and genomic complexity of SARS-CoV-2 in Rio Grande do Sul, the southernmost state in Brazil. Most samples sequenced belonged to the B.1.1.28 (E484K) lineage, demonstrating its widespread dispersion. We were the first to identify two independent events of co-infection caused by the occurrence of B.1.1.28 (E484K) with either B.1.1.248 or B.1.91 lineages. Also, clustering analysis revealed the occurrence of a novel cluster of samples circulating in the state (named VUI-NP13L) characterized by 12 lineage-defining mutations. In light of the evidence for E484K dispersion, co-infection and emergence of VUI-NP13 L in Rio Grande do Sul, we reaffirm the importance of establishing strict and effective social distancing measures to counter the spread of potentially more hazardous SARS-CoV-2 strains.

Virus-host coexistence in phytoplankton through the genomic lens.

Virus-microbe interactions in the ocean are commonly described by "boom and bust" dynamics, whereby a numerically dominant microorganism is lysed and replaced by a virus-resistant one. Here, we isolated a microalga strain and its infective dsDNA virus whose dynamics are characterized instead by parallel growth of both the microalga and the virus. Experimental evolution of clonal lines revealed that this viral production originates from the lysis of a minority of virus-susceptible cells, which are regenerated from resistant cells. Whole-genome sequencing demonstrated that this resistant-susceptible switch involved a large deletion on one chromosome. Mathematical modeling explained how the switch maintains stable microalga-virus population dynamics consistent with their observed growth pattern. Comparative genomics confirmed an ancient origin of this "accordion" chromosome despite a lack of sequence conservation. Together, our results show how dynamic genomic rearrangements may account for a previously overlooked coexistence mechanism in microalgae-virus interactions.

Genome Resolved Biogeography of Mamiellales.

Among marine phytoplankton, Mamiellales encompass several species from the genera Micromonas, Ostreococcus and Bathycoccus, which are important contributors to primary production. Previous studies based on single gene markers described their wide geographical distribution but led to discussion because of the uneven taxonomic resolution of the method. Here, we leverage genome sequences for six Mamiellales species, two from each genus Micromonas, Ostreococcus and Bathycoccus, to investigate their distribution across 133 stations sampled during the Tara Oceans expedition. Our study confirms the cosmopolitan distribution of Mamiellales and further suggests non-random distribution of species, with two triplets of co-occurring genomes associated with different temperatures: Ostreococcuslucimarinus, Bathycoccusprasinos and Micromonaspusilla were found in colder waters, whereas Ostreococcus spp. RCC809, Bathycoccus spp. TOSAG39-1 and Micromonascommoda were more abundant in warmer conditions. We also report the distribution of the two candidate mating-types of Ostreococcus for which the frequency of sexual reproduction was previously assumed to be very low. Indeed, both mating types were systematically detected together in agreement with either frequent sexual reproduction or the high prevalence of a diploid stage. Altogether, these analyses provide novel insights into Mamiellales' biogeography and raise novel testable hypotheses about their life cycle and ecology.

Single cell ecogenomics reveals mating types of individual cells and ssDNA viral infections in the smallest photosynthetic eukaryotes.

Planktonic photosynthetic organisms of the class Mamiellophyceae include the smallest eukaryotes (less than 2 µm), are globally distributed and form the basis of coastal marine ecosystems. Eight complete fully annotated 13-22 Mb genomes from three genera, Ostreococcus, Bathycoccus and Micromonas, are available from previously isolated clonal cultured strains and provide an ideal resource to explore the scope and challenges of analysing single cell amplified genomes (SAGs) isolated from a natural environment. We assembled data from 12 SAGs sampled during the Tara Oceans expedition to gain biological insights about their in situ ecology, which might be lost by isolation and strain culture. Although the assembled nuclear genomes were incomplete, they were large enough to infer the mating types of four Ostreococcus SAGs. The systematic occurrence of sequences from the mitochondria and chloroplast, representing less than 3% of the total cell's DNA, intimates that SAGs provide suitable substrates for detection of non-target sequences, such as those of virions. Analysis of the non-Mamiellophyceae assemblies, following filtering out cross-contaminations during the sequencing process, revealed two novel 1.6 and 1.8 kb circular DNA viruses, and the presence of specific Bacterial and Oomycete sequences suggests that these organisms might co-occur with the Mamiellales. This article is part of a discussion meeting issue 'Single cell ecology'.