Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta)

Abstract

Porphyra umbilicalis (laver) belongs to an ancient group of red algae (Bangiophyceae), is harvested for human food, and thrives in the harsh conditions of the upper intertidal zone. Here we present the 87.7-Mbp haploid Porphyra genome (65.8% G + C content, 13,125 gene loci) and elucidate traits that inform our understanding of the biology of red algae as one of the few multicellular eukaryotic lineages. Novel features of the Porphyra genome shared by other red algae relate to the cytoskeleton, calcium signaling, the cell cycle, and stress-tolerance mechanisms including photoprotection. Cytoskeletal motor proteins in Porphyra are restricted to a small set of kinesins that appear to be the only universal cytoskeletal motors within the red algae. Dynein motors are absent, and most red algae, including Porphyra, lack myosin. This surprisingly minimal cytoskeleton offers a potential explanation for why red algal cells and multicellular structures are more limited in size than in most multicellular lineages. Additional discoveries further relating to the stress tolerance of bangiophytes include ancestral enzymes for sulfation of the hydrophilic galactan-rich cell wall, evidence for mannan synthesis that originated before the divergence of green and red algae, and a high capacity for nutrient uptake. Our analyses provide a comprehensive understanding of the red algae, which are both commercially important and have played a major role in the evolution of other algal groups through secondary endosymbioses.cytoskeleton | calcium-signaling | carbohydrate-active enzymes | stress tolerance | vitamin B 12T he red algae are one of the founding groups of photosynthetic eukaryotes (Archaeplastida) and among the few multicellular lineages within Eukarya. A red algal plastid, acquired through secondary endosymbiosis, supports carbon fixation, fatty acid synthesis, and other metabolic needs in many other algal groups in ways that are consequential. For example, diatoms and haptophytes have strong biogeochemical effects; apicomplexans cause human disease (e.g., malaria); and dinoflagellates include both coral symbionts and toxin-producing "red tides" (1). The evolutionary processes that produced the Archaeplastida and secondary algal lineages remain under investigation (2-5), but it is clear that both nuclear and plastid genes from the ancestral red algae have contributed dramatically to broader eukaryotic evolution and diversity. Consequently, the imprint of red algal metabolism on the Earth's climate system, aquatic foodwebs, and

Evolution and expression of core SWI/SNF genes in red algae

“…), BLAST searches of both gene models and extensive EST data from the P. umbilicalis genome (Brawley et al. ) returned one sequence with significant similarity to yeast, human, Arabidopsis , and Cyandioschyzon SWI3 homologs (Fig. C).…”

“…) and RNA‐seq (Brawley et al. ) data. Although no gene model has been annotated from the Pyropia genome (Nakamura et al.…”

“…In an effort to expand comparative SWI/SNF analyses, particularly to additional florideophytes and members of the SRCP clade (Brawley et al. ), eight expansive EST data sets also were queried (Table ). When no sequence with significant similarity to the three validated sequences was found, unvalidated but strongly conserved sequences from more closely related red algae also were used as BLAST queries to look for potentially more divergent homologs.…”

“…, Brawley et al. ) were analyzed for expression of SWI/SNF genes from materials harvested under different developmental and environmental conditions. Porphyra umbilicalis RNA‐seq reads generated from vegetative blade centers (NCBI, SRX115569), developing neutral spores (SRX115570) and mature spores (SRX115571) were examined.…”

“…In all that time, however, no member of the Rhodophyta has managed to attain the kinds of cellular and tissue‐level differentiation present in most other eukaryotic lineages that have evolved large, multicellular forms (Murray and Dixon , Brawley et al. ). The most developmentally complex florideophyte red algae have multiaxial filamentous construction, reinforced by secondary connections (pit plugs) between filamentous axes, forming pseudoparenchyma that mimics tissues and stabilizes leaf‐, stem‐ and bulb‐like structures (Coomans and Hommersand ).…”