Insights into the red algae and eukaryotic evolution from the genome of $\textit{Porphyra umbilicalis}$ (Bangiophyceae, Rhodophyta)

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.

The work conducted by the US Department of Energy (DOE) Joint Genome Institute, a DOE Office of Science User Facility, was supported by the Office of Science of the US DOE under Contract DE-AC02-05CH11231 (to S.H.B., E.G., A.R.G., and J.W.S.). Other major research support was provided by NSF 0929558 (to S.H.B. and A.R.G.); National Oceanic and Atmospheric Administration (NOAA) Contract NA060AR4170108 (to S.H.B.); German Research Foundation Grant Mi373/12-2 of FOR1261 (to M.M.); the French National Research Agency under IDEALG Grants ANR-10- BTBR-04-02 and 04-04 “Investissements d’avenir, Biotechnologies-Bioressources” (to J.C., E.F.-B., G.M., and S.M.D.); the New Hampshire Agricultural Experiment Station, Scientific Contribution No. 2694, supported by the US Department of Agriculture/National Institute of Food and Agriculture Hatch Project 1004051 (to A.S.K. and Y.C.); the Biotechnology and Biological Sciences Research Council (BBSRC BB/1013164/1) of the United Kingdom and European Union FP7 Marie Curie ITN Photo.Comm 317184 (to A.G.S. and K.E.H.); the Office of Biological and Environmental Research of the US DOE (C.E.B.-H.); the Connecticut Sea Grant College Program (R/A-38) and the NOAA National Marine Aquaculture Initiative (C.Y.); the NIH MCB 1244593 (to H.V.G.); NSF and NIH Grants NSF-MCB 1412738, NIH P20GM103418, and NIH P20GM103638 (to B.J.S.C.O.); NSF Graduate Research Fellowship under Grant 1247393 (to B.N.S.); the UK Natural Environment Research Council IOF Pump-priming + scheme Grant NE/L013223/1 (to C.M.M.G. and Y.B.); NOAA Contract NA14OAR4170072 (to S.H.B.); and The Great Barrier Reef Foundation, Australian Research Council (DP150101875) and a University of Queensland Early Career Researcher Grant (to C.X.C.).