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

Susan H. Brawley, Nicolas A. Blouin, Elizabeth Ficko-Blean, Glen L. Wheeler, Martin Lohr, Holly V. Goodson, Jerry W. Jenkins, Crysten E. Blaby-Haas, Katherine E. Helliwell, Cheong Xin Chan, Tara N. Marriage, Debashish Bhattacharya, Anita S. Klein, Yacine Badis, Juliet Brodie, Yuanyu Cao, Jonas Collén, Simon M. Dittami, Claire M. M. Gachon, Beverley R. Green, Steven J. Karpowicz, Jay W. Kim, Ulrich Johan Kudahl, Senjie Lin, Gurvan Michel, Maria Mittag, Bradley J. S. C. Olson, Jasmyn L. Pangilinan, Yi Peng, Huan Qiu, Shengqiang Shu, John T. Singer, Alison G. Smith, Brittany N. Sprecher, Volker Wagner, Wenfei Wang, Zhi-Yong Wang, Juying Yan, Charles Yarish, Simone Zäuner-Riek, Yunyun Zhuang, Yong Zou, Erika A. Lindquist, Jane Grimwood, Kerrie W. Barry, Daniel S. Rokhsar, Jeremy Schmutz, John W. Stiller, Arthur R. Grossman, Simon E. Prochnik

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.