Jonas Collén

The Ectocarpus genome and the independent evolution of multicellularity in brown algae

Brown algae (Phaeophyceae) are complex photosynthetic organisms with a very different evolutionary history to green plants, to which they are only distantly related. These seaweeds are the dominant species in rocky coastal ecosystems and they exhibit many interesting adaptations to these, often harsh, environments. Brown algae are also one of only a small number of eukaryotic lineages that have evolved complex multicellularity (Fig. 1). We report the 214 million base pair (Mbp) genome sequence of the filamentous seaweed Ectocarpus siliculosus (Dillwyn) Lyngbye, a model organism for brown algae, closely related to the kelps (Fig. 1). Genome features such as the presence of an extended set of light-harvesting and pigment biosynthesis genes and new metabolic processes such as halide metabolism help explain the ability of this organism to cope with the highly variable tidal environment. The evolution of multicellularity in this lineage is correlated with the presence of a rich array of signal transduction genes. Of particular interest is the presence of a family of receptor kinases, as the independent evolution of related molecules has been linked with the emergence of multicellularity in both the animal and green plant lineages. The Ectocarpus genome sequence represents an important step towards developing this organism as a model species, providing the possibility to combine genomic and genetic approaches to explore these and other aspects of brown algal biology further.

Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida

Red seaweeds are key components of coastal ecosystems and are economically important as food and as a source of gelling agents, but their genes and genomes have received little attention. Here we report the sequencing of the 105-Mbp genome of the florideophyte Chondrus crispus (Irish moss) and the annotation of the 9,606 genes. The genome features an unusual structure characterized by gene-dense regions surrounded by repeat-rich regions dominated by transposable elements. Despite its fairly large size, this genome shows features typical of compact genomes, e.g., on average only 0.3 introns per gene, short introns, low median distance between genes, small gene families, and no indication of large-scale genome duplication. The genome also gives insights into the metabolism of marine red algae and adaptations to the marine environment, including genes related to halogen metabolism, oxylipins, and multicellularity (microRNA processing and transcription factors). Particularly interesting are features related to carbohydrate metabolism, which include a minimalistic gene set for starch biosynthesis, the presence of cellulose synthases acquired before the primary endosymbiosis showing the polyphyly of cellulose synthesis in Archaeplastida, and cellulases absent in terrestrial plants as well as the occurrence of a mannosylglycerate synthase potentially originating from a marine bacterium. To explain the observations on genome structure and gene content, we propose an evolutionary scenario involving an ancestral red alga that was driven by early ecological forces to lose genes, introns, and intergenetic DNA; this loss was followed by an expansion of genome size as a consequence of activity of transposable elements.

The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea

Seagrasses colonized the sea on at least three independent occasions to form the basis of one of the most productive and widespread coastal ecosystems on the planet. Here we report the genome of Zostera marina (L.), the first, to our knowledge, marine angiosperm to be fully sequenced. This reveals unique insights into the genomic losses and gains involved in achieving the structural and physiological adaptations required for its marine lifestyle, arguably the most severe habitat shift ever accomplished by flowering plants. Key angiosperm innovations that were lost include the entire repertoire of stomatal genes, genes involved in the synthesis of terpenoids and ethylene signalling, and genes for ultraviolet protection and phytochromes for far-red sensing. Seagrasses have also regained functions enabling them to adjust to full salinity. Their cell walls contain all of the polysaccharides typical of land plants, but also contain polyanionic, low-methylated pectins and sulfated galactans, a feature shared with the cell walls of all macroalgae and that is important for ion homoeostasis, nutrient uptake and O2/CO2 exchange through leaf epidermal cells. The Z. marina genome resource will markedly advance a wide range of functional ecological studies from adaptation of marine ecosystems under climate warming, to unravelling the mechanisms of osmoregulation under high salinities that may further inform our understanding of the evolution of salt tolerance in crop plants.

Evolution of Red Algal Plastid Genomes: Ancient Architectures, Introns, Horizontal Gene Transfer, and Taxonomic Utility of Plastid Markers

Red algae have the most gene-rich plastid genomes known, but despite their evolutionary importance these genomes remain poorly sampled. Here we characterize three complete and one partial plastid genome from a diverse range of florideophytes. By unifying annotations across all available red algal plastid genomes we show they all share a highly compact and slowly-evolving architecture and uniquely rich gene complements. Both chromosome structure and gene content have changed very little during red algal diversification, and suggest that plastid-to nucleus gene transfers have been rare. Despite their ancient character, however, the red algal plastids also contain several unprecedented features, including a group II intron in a tRNA-Met gene that encodes the first example of red algal plastid intron maturase – a feature uniquely shared among florideophytes. We also identify a rare case of a horizontally-acquired proteobacterial operon, and propose this operon may have been recruited for plastid function and potentially replaced a nucleus-encoded plastid-targeted paralogue. Plastid genome phylogenies yield a fully resolved tree and suggest that plastid DNA is a useful tool for resolving red algal relationships. Lastly, we estimate the evolutionary rates among more than 200 plastid genes, and assess their usefulness for species and subspecies taxonomy by comparison to well-established barcoding markers such as cox1 and rbcL. Overall, these data demonstrates that red algal plastid genomes are easily obtainable using high-throughput sequencing of total genomic DNA, interesting from evolutionary perspectives, and promising in resolving red algal relationships at evolutionarily-deep and species/subspecies levels.

GENETIC POPULATION STRUCTURE AND MATING SYSTEM IN CHONDRUS CRISPUS (RHODOPHYTA)1

Chondrus crispus Stackh. has been intensely studied, yet no study to date has elucidated its population structure or mating system despite many populations in which there was a haploid bias and lack of male gametophytes. Therefore, 12 nuclear microsatellite loci were identified in this red alga. Microsatellite markers were developed and tested against a panel of specimens collected from two shore levels at two sites in Brittany, France: Pointe de Primel and Pointe de la Jument, Concarneau. Single locus genetic determinism was verified at eight polymorphic loci, as only one band was observed for haploid genotypes, whereas one or two bands were observed for diploids. These markers enabled the detection of unique genotypes within sampled populations, indicating that very few fronds shared the same multilocus genotype. This finding suggests that asexual reproduction was not the prevailing mode of reproduction. In addition, we explored the hierarchical population structure showing that gene flow is restricted at small spatial scales (<50 m) between upper and lower Chondrus‐range populations within a shore. Sexual reproduction predominated in the populations of C. crispus studied, but probably due to fine‐scale spatial substructuring, inbreeding was also significant. In conclusion, this study reveals that fine‐scale genetic variation is of major importance in C. crispus, suggesting that differences between microhabitats should be essential in understanding evolutionary processes in this species.

Porphyra: Complex Life Histories in a Harsh Environment: P. umbilicalis, an Intertidal Red Alga for Genomic Analysis

Porphyra encompasses a large group of multicellular red algae that have a prominent gametophytic phase. The complex, heteromorphic life history of species in this genus, their remarkable resilience to high light and desiccation, ancient fossil records, and value as human food (e.g., laver, nori), make Porphyra a compelling model for genome sequencing. Sequencing of the nuclear genome of Porphyra umbilicalis from the northwestern Atlantic is currently in process. The ∼270 Mb genome of this alga is much larger than that of the unicellular acidophilic Cyanidioschyzon merolae (16.5 Mb), the only rhodophyte for which there is a fully sequenced genome, and is approximately twice as large as the Arabidopsis genome. Future analyses of the P. umbilicalis genome should provide opportunities for researchers to (1) develop an increased understanding of the ways in which these algae have adapted to severe physiological stresses, (2) elucidate the molecular features of development through the complex life history, and (3) define key components required for the transition of growth from a single cell to a multicellular organism.

Chondrus crispus – A Present and Historical Model Organism for Red Seaweeds

Abstract Chondrus crispus, or Irish moss, is a common edible red seaweed that can be found on rocky shores in the Northern Atlantic. The cell wall contains carrageenan and C. crispus is the original source of this commercially used thickener. Because of the ecological and economic importance of this red alga a relatively important research literature exists and one of the recent achievements in C. crispus research is the sequencing of its genome. In this chapter we review some of the literature with the aim to promote C. crispus as a model organism for florideophyte red seaweeds. We consider subjects like commercial and historical uses, ecology, genetics, population structure, mating systems, physiology, cell wall biology and genomics.

The Ectocarpus Genome and Brown Algal Genomics

Brown algae are important organisms both because of their key ecological roles in coastal ecosystems and because of the remarkable biological features that they have acquired during their unusual evolutionary history. The recent sequencing of the complete genome of the filamentous brown alga Ectocarpus has provided unprecedented access to the molecular processes that underlie brown algal biology. Analysis of the genome sequence, which exhibits several unusual structural features, identified genes that are predicted to play key roles in several aspects of brown algal metabolism, in the construction of the multicellular bodyplan and in resistance to biotic and abiotic stresses. Information from the genome sequence is currently being used in combination with other genomic, genetic and biochemical tools to further investigate these and other aspects of brown algal biology at the molecular level. Here, we review some of the major discoveries that emerged from the analysis of the Ectocarpus genome sequence, with a particular focus on the unusual genome structure, inferences about brown algal evolution and novel aspects of brown algal metabolism.

The Ectocarpus Genome and Brown Algal Genomics: The Ectocarpus Genome Consortium

Brown algae are important organisms both because of their key ecological roles in coastal ecosystems and because of the remarkable biological features that they have acquired during their unusual evolutionary history. The recent sequencing of the complete genome of the filamentous brown alga Ectocarpus has provided unprecedented access to the molecular processes that underlie brown algal biology. Analysis of the genome sequence, which exhibits several unusual structural features, identified genes that are predicted to play key roles in several aspects of brown algal metabolism, in the construction of the multicellular bodyplan and in resistance to biotic and abiotic stresses. Information from the genome sequence is currently being used in combination with other genomic, genetic and biochemical tools to further investigate these and other aspects of brown algal biology at the molecular level. Here, we review some of the major discoveries that emerged from the analysis of the Ectocarpus genome sequence, with a particular focus on the unusual genome structure, inferences about brown algal evolution and novel aspects of brown algal metabolism.

Independent Emergence of Complex Multicellularity in the Brown and Red Algae

Brown and red macroalgae represent two of only five eukaryotic groups that have independently evolved complex multicellularity. Compared with animals and land plants, very little is known about the molecular mechanisms underlying multicellular development in the two macroalgal groups, but the recent publication of complete genome sequences for both of these lineages has been a first step towards changing this situation. Comparisons of these genomes with those of other multicellular and unicellular organisms have identified a number of features that may be related to the transitions to complex multicellularity in these macroalgal lineages. One particularly striking feature of the brown algae, for example, is the emergence of a family of membrane-spanning receptor kinases, a class of molecules that is also thought to have been important for the transition to complex multicellularity in animals and land plants. Surprisingly, the genomes of the brown alga Ectocarpus and the red alga Chondrus are remarkably different at the structural level, despite the fact that both organisms represent lineages that have evolved multicellularity as sedentary organisms in the seashore environment. Current efforts to identify and characterise developmental regulators in macroalgae are expected to enrich comparisons with other complex multicellular lineages.