Pre-domestication bottlenecks of the cultivated seaweed Gracilaria chilensis.

Gracilaria chilensis is the main cultivated seaweed in Chile. The low genetic diversity observed in the Chilean populations has been associated with the over-exploitation of natural beds and/or the founder effect that occurred during post-glacial colonization from New Zealand. How these processes have affected its evolutionary trajectory before farming and incipient domestication is poorly understood. In this study, we used 2232 single nucleotide polymorphisms (SNPs) to assess how the species' evolutionary history in New Zealand (its region of origin), the founder effect linked to transoceanic dispersion and colonization of South America, and the recent over-exploitation of natural populations have influenced the genetic architecture of G. chilensis in Chile. The contrasting patterns of genetic diversity and structure observed between the two main islands in New Zealand attest to the important effects of Quaternary glacial cycles on G. chilensis. Approximate Bayesian Computation (ABC) analyses indicated that Chatham Island and South America were colonized independently near the end of the Last Glacial Maximum and emphasized the importance of coastal and oceanic currents during that period. Furthermore, ABC analyses inferred the existence of a recent and strong genetic bottleneck in Chile, matching the period of over-exploitation of the natural beds during the 1970s, followed by rapid demographic expansion linked to active clonal propagation used in farming. Recurrent genetic bottlenecks strongly eroded the genetic diversity of G. chilensis prior to its cultivation, raising important challenges for the management of genetic resources in this incipiently domesticated species.

Intraorganismal genetic heterogeneity as a source of genetic variation in modular macroalgae.

Genetic diversity is considered a key factor of population survival and evolution, especially in changing environments. Genetic diversity arises from mutations in the DNA sequence of cell lines and from there it reaches the level of organisms, populations, and regions. However, many previous studies have not considered the organism architecture or pattern of thallus construction, ignoring the potential genetic complexities that intraorganismal genetic heterogeneity could generate in modular organisms. In seaweeds, modularity and clonality exist in many species. Modular organization has been related to advantages in terms of rapid construction and recovery after the loss of individual modules, which have their own demographic properties as they generate, mature, senesce, and die. Based on recent evidence from the literature, we suggest that modules also have their own genetic properties. Specifically, modular seaweeds have two possible sources of genetic diversity at the individual level: the heterozygosity of the genotypes composing the genet, and genetic heterogeneity among the modules within a genet (i.e., intraclonal genetic variability). Both sources of genetic diversity can have ecological and evolutionary consequences, and most of them must be considered in research on modular seaweeds. Linking intraorganismal genetic diversity with clonal architecture and propagation styles may help us to understand important ecological and evolutionary processes such as speciation modes, invasive capacities, or farming potential.

Expression profile of desiccation tolerance factors in intertidal seaweed species during the tidal cycle.

MAIN CONCLUSION: The transcriptional modulation of desiccation tolerance factors in P. orbicularis explains its successful recuperation after water deficit. Differential responses to air exposure clarify seaweed distribution along intertidal rocky zones. Desiccation-tolerant seaweed species, such as Pyropia orbicularis, can tolerate near 96% water loss during air exposure. To understand the phenotypic plasticity of P. orbicularis to desiccation, several tolerance factors were assessed by RT-qPCR, Western-blot analysis, and enzymatic assays during the natural desiccation-rehydration cycle. Comparative enzymatic analyses were used to evidence differential responses between P. orbicularis and desiccation-sensitive species. The results showed that during desiccation, the relative mRNA levels of genes associated with basal metabolism [trehalose phosphate synthase (tps) and pyruvate dehydrogenase (pdh)] were overexpressed in P. orbicularis. Transcript levels related to antioxidant metabolism [peroxiredoxin (prx); thioredoxin (trx); catalase (cat); lipoxygenase (lox); ferredoxin (fnr); glutathione S-transferase (gst)], cellular detoxification [ABC transporter (abc) and ubiquitin (ubq)], and signal transduction [calmodulin (cam)] increased approximately 15- to 20-fold, with the majority returning to basal levels during the final hours of rehydration. In contrast, actin (act) and transcription factor 1 (tf1) transcripts were down-regulated. ABC transporter protein levels increased in P. orbicularis during desiccation, whereas PRX transcripts decreased. The antioxidant enzymes showed higher specific activity in P. orbicularis under desiccation, and sensitive species exhibited enzymatic inactivation and scarce ABC and PRX protein detection following prolonged desiccation. In conclusion, the reported findings contribute towards understanding the ecological distribution of intertidal seaweeds at the molecular and functional levels.

Coalescing red algae exhibit noninvasive, reversible chimerism.

Chimerism is produced by the somatic fusion of two or more genetically distinct conspecific individuals. In animals, the main cost of fusion is competition between genetically different cell lineages and the probability of original cell line replacement by more competitive invasive lines, which limits its natural frequency (3%-5%). In red and brown seaweeds, chimerism is widespread (27%-53%), seemingly without the negative outcomes described for animals. The rigidity of cell walls in macroalgae prevents cell motility and invasions. In addition, in moving waters, most somatic fusions involve the holdfast. Histological observations in laboratory-built bicolor macroalgal chimeras indicated that upright axes emerge from the base of plants by proliferation and vertical growth of discrete cell groups that include one or just a few of the cell lineages occurring in the holdfasts. Laboratory experiments showed growth competition between cell lineages, thus explaining lineage segregation during growth along originally chimeric erect axes. Genotyping of the axes showed more heterogeneous tissues basally, but apically more homogeneous ones, generating a vertical gradient of allele abundance and diversity. The few chimeric primary branches produced, eventually became homogenous after repeated branching. Therefore, coalescing macroagae exhibit a unique pattern of post-fusion growth, with the capacity to reverse chimerism. This pattern is significantly different from those in animals and land plants, suggesting chimerism is a biologically heterogeneous concept.

Delimitating cryptic species in the Gracilaria domingensis complex (Gracilariaceae, Rhodophyta) using molecular and morphological data.

Species in the genus Gracilaria that display conspicuously flattened vegetative morphologies are a taxonomically challenging group of marine benthic red algae. This is a result of their species richness, morphological similarity, and broad phenotypic plasticity. Within this group, the Gracilaria domingensis complex is one of the most common, conspicuous, and morphologically variable species along the tropical western Atlantic Ocean. Previous research has identified that members of this complex belong to two distantly related clades. However, despite this increased phylogentic resolution, species delimitations within each of these clades remain unclear. Our study assessed the species diversity within this difficult complex using morphological and molecular data from three genetic markers (cox1, UPA, and rbcL). We additionally applied six single-marker species delimitation methods (SDM: ABGD, GMYCs, GMYCm, SPN, bPTP, and PTP) to rbcL, which were largely in agreement regarding species delimitation. These results, combined with our analysis of morphology, indicate that the G. domingensis complex includes seven distinct species, each of which are not all most closely related: G. cervicornis; a ressurected G. ferox; G. apiculata subsp. apiculata; a new species, Gracilaria baiana sp. nov.; G. intermedia subsp. intermedia; G. venezuelensis; and G. domingensis sensu stricto, which includes the later heterotypic synonym, G. yoneshigueana. Our study demonstrates the value of multipronged strategies, including the use of both molecular and morphological approaches, to decipher cryptic species of red algae.

Tracing the trans-pacific evolutionary history of a domesticated Seaweed (Gracilaria chilensis) with archaeological and genetic data.

The history of a domesticated marine macroalga is studied using archaeological, phylogeographic and population genetic tools. Phylogeographic and population genetic analyses demonstrated that the cultivated red alga Gracilaria chilensis colonised the Chilean coast from New Zealand. Combining archaeological observations with phylogeographic data provided evidence that exchanges between New Zealand and Chile have occurred at least before the Holocene, likely at the end of the Last Glacial Maximum (LGM) and we suggest that migration probably occurred via rafting. Furthermore, the remarkably low microsatellite diversity found in the Chilean populations compared to those in New Zealand is consistent with a recent genetic bottleneck as a result of over-exploitation of natural populations and/or the process of domestication. Therefore, the aquaculture of this seaweed, based essentially on clonal propagation, is occurring from genetically depressed populations and may be driving the species to an extinction vortex in Chile.

Evidence of macroalgal colonization on newly ice-free areas following glacial retreat in Potter Cove (South Shetland Islands), Antarctica.

Climate warming has been related to glacial retreat along the Western Antarctic Peninsula. Over the last years, a visible melting of Fourcade Glacier (Potter Cove, South Shetland Islands) has exposed newly ice-free hard bottom areas available for benthic colonization. However, ice melting produces a reduction of light penetration due to an increase of sediment input and higher ice impact. Seventeen years ago, the coastal sites close to the glacier cliffs were devoid of macroalgae. Are the newly ice-free areas suitable for macroalgal colonization? To tackle this question, underwater video transects were performed at six newly ice-free areas with different degree of glacial influence. Macroalgae were found in all sites, even in close proximity to the retreating glacier. We can show that: 1. The complexity of the macroalgal community is positively correlated to the elapsed time from the ice retreat, 2. Algae development depends on the optical conditions and the sediment input in the water column; some species are limited by light availability, 3. Macroalgal colonization is negatively affected by the ice disturbance, 4. The colonization is determined by the size and type of substrate and by the slope of the bottom. As macroalgae are probably one of the main energy sources for the benthos, an expansion of the macroalgal distribution can be expected to affect the matter and energy fluxes in Potter Cove ecosystem.

Transcriptomic analysis of the red seaweed Laurencia dendroidea (Florideophyceae, Rhodophyta) and its microbiome.

BACKGROUND: Seaweeds of the Laurencia genus have a broad geographic distribution and are largely recognized as important sources of secondary metabolites, mainly halogenated compounds exhibiting diverse potential pharmacological activities and relevant ecological role as anti-epibiosis. Host-microbe interaction is a driving force for co-evolution in the marine environment, but molecular studies of seaweed-associated microbial communities are still rare. Despite the large amount of research describing the chemical compositions of Laurencia species, the genetic knowledge regarding this genus is currently restricted to taxonomic markers and general genome features. In this work we analyze the transcriptomic profile of L. dendroidea J. Agardh, unveil the genes involved on the biosynthesis of terpenoid compounds in this seaweed and explore the interactions between this host and its associated microbiome. RESULTS: A total of 6 transcriptomes were obtained from specimens of L. dendroidea sampled in three different coastal locations of the Rio de Janeiro state. Functional annotations revealed predominantly basic cellular metabolic pathways. Bacteria was the dominant active group in the microbiome of L. dendroidea, standing out nitrogen fixing Cyanobacteria and aerobic heterotrophic Proteobacteria. The analysis of the relative contribution of each domain highlighted bacterial features related to glycolysis, lipid and polysaccharide breakdown, and also recognition of seaweed surface and establishment of biofilm. Eukaryotic transcripts, on the other hand, were associated with photosynthesis, synthesis of carbohydrate reserves, and defense mechanisms, including the biosynthesis of terpenoids through the mevalonate-independent pathway. CONCLUSIONS: This work describes the first transcriptomic profile of the red seaweed L. dendroidea, increasing the knowledge about ESTs from the Florideophyceae algal class. Our data suggest an important role for L. dendroidea in the primary production of the holobiont and the role of Bacteria as consumers of organic matter and possibly also as nitrogen source. Furthermore, this seaweed expressed sequences related to terpene biosynthesis, including the complete mevalonate-independent pathway, which offers new possibilities for biotechnological applications using secondary metabolites from L. dendroidea.