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Title: Insights into the red algae and eukaryotic evolution from the genome of 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 amore » 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.« less
Authors:
 [1] ;  [2] ;  [3] ;  [4] ;  [5] ;  [6] ;  [7] ;  [8] ;  [4] ;  [9] ;  [10] ; ORCiD logo [11] ;  [12] ;  [13] ;  [14] ;  [12] ;  [15] ;  [15] ;  [13] ;  [16] more »;  [17] ;  [18] ;  [19] ;  [20] ;  [15] ;  [21] ;  [22] ;  [23] ;  [23] ;  [24] ;  [23] ;  [25] ; ORCiD logo [26] ;  [20] ;  [21] ;  [27] ;  [28] ;  [23] ;  [29] ;  [30] ;  [20] ;  [21] ;  [23] ;  [7] ;  [23] ;  [23] ;  [7] ;  [31] ;  [28] ;  [23] « less
  1. University of Maine, Orono (Maine). School of Marine Sciences
  2. University of Maine, Orono (Maine). School of Marine Sciences; Univ. of Wyoming, Laramie, WY (United States). Department of Molecular Biology
  3. Sorbonne Universites, Universite Pierre and Marie Curie Paris (France). Integrative Biology of Marine Models, Station Biologique de Roscoff
  4. Marine Biological Association of the United Kingdom, Plymouth (United Kingdom)
  5. Johannes Gutenberg-Universitat Mainz (Germany). Institute for Molecular Biology
  6. University of Notre Dame, South Bend, IN (United States). Department of Chemistry & Biochemistry
  7. HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  8. Brookhaven National Lab. (BNL), Upton, NY (United States). Biology Dept.
  9. Univ. of Queensland, Brisbane (Australia). Institute for Molecular Bioscience and School of Chemistry and Molecular Biosciences
  10. Kansas State Univ., Manhattan, KS (United States). Division of Biology
  11. Rutgers Univ., New Brunswick, NJ (United States). Department of Ecology, Evolution & Natural Resources
  12. Univ. of New Hampshire, Durham, NH (United States). Department of Biological Sciences
  13. Scottish Marine Institute (United Kingdom). Scottish Association for Marine Sciences
  14. Natural History Museum, Department of Life Sciences, London (United Kingdom)
  15. Sorbonne Universites, Universite Pierre and Marie Curie Paris (France). Integrative Biology of Marine Models, Station Biologique de Roscoff
  16. University of British Columbia, Vancouver BC (Canada). Department of Botany
  17. Tau Biosciences LLC, Edmond, OK (United States)
  18. University of California, Santa Cruz, CA (United States). Department of Biomolecular Engineering
  19. University of Cambridge (United Kingdom). Department of Plant Sciences
  20. University of Connecticut, Groton, CT (United States). Department of Marine Sciences
  21. Friedrich-Schiller University, Jena (Germany). Institute of General Botany and Plant Phisiology
  22. Kansas State University, Manhattan, KS (United States). Division of Biology
  23. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  24. Rutgers University, New Brunswick, NJ (United States). Department of Ecology, Evolution & Natural Resources
  25. University of Maine, Orono, ME (United States). Department of Molecular & Biomedical Science
  26. University of Cambridge (United Kingdom). Dept. of Plant Sciences
  27. Fujian Agriculture and Forestry University, Fuzhou (China). Basic Forestry and Proteomics Research Center, HIST
  28. Carnegie Institution for Science, Stanford, CA (United States). Dept. of Plant Science
  29. University of Connecticut, Stamford, CT (United States). Department of Ecology & Evolutionary Biology
  30. University of Bonn (Germany). Institute of Molecular Physiology and Biotechnology
  31. East Carolina University, Greenville, NC (United States). Department of Biology
Publication Date:
Report Number(s):
BNL-114055-2017-JA
Journal ID: ISSN 0027-8424
Grant/Contract Number:
SC0012704; AC02-05CH11231
Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 114; Journal Issue: 31; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Research Org:
Brookhaven National Laboratory (BNL), Upton, NY (United States)
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; antioxidants; carbohydrate-active enzymes (CAZymes); cyclin D; iron-uptake; kinesin; mannan biosynthesis; mycosporine-like amino acids (MAAs); septins; sulfated galactans; vitamin B12
OSTI Identifier:
1376126

Brawley, Susan H., Blouin, Nicolas A., Ficko-Blean, Elizabeth, Wheeler, Glen L., Lohr, Martin, Goodson, Holly V., Jenkins, Jerry W., Blaby-Haas, Crysten E., Helliwell, Katherine E., Chan, Cheong Xin, Marriage, Tara N., Bhattacharya, Debashish, Klein, Anita S., Badis, Yacine, Brodie, Juliet, Cao, Yuanyu, Collén, Jonas, Dittami, Simon M., Gachon, Claire M. M., Green, Beverley R., Karpowicz, Steven J., Kim, Jay W., Kudahl, Ulrich Johan, Lin, Senjie, Michel, Gurvan, Mittag, Maria, Olson, Bradley J. S. C., Pangilinan, Jasmyn L., Peng, Yi, Qiu, Huan, Shu, Shengqiang, Singer, John T., Smith, Alison G., Sprecher, Brittany N., Wagner, Volker, Wang, Wenfei, Wang, Zhi-Yong, Yan, Juying, Yarish, Charles, Zäuner-Riek, Simone, Zhuang, Yunyun, Zou, Yong, Lindquist, Erika A., Grimwood, Jane, Barry, Kerrie W., Rokhsar, Daniel S., Schmutz, Jeremy, Stiller, John W., Grossman, Arthur R., and Prochnik, Simon E.. Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta). United States: N. p., Web. doi:10.1073/pnas.1703088114.
Brawley, Susan H., Blouin, Nicolas A., Ficko-Blean, Elizabeth, Wheeler, Glen L., Lohr, Martin, Goodson, Holly V., Jenkins, Jerry W., Blaby-Haas, Crysten E., Helliwell, Katherine E., Chan, Cheong Xin, Marriage, Tara N., Bhattacharya, Debashish, Klein, Anita S., Badis, Yacine, Brodie, Juliet, Cao, Yuanyu, Collén, Jonas, Dittami, Simon M., Gachon, Claire M. M., Green, Beverley R., Karpowicz, Steven J., Kim, Jay W., Kudahl, Ulrich Johan, Lin, Senjie, Michel, Gurvan, Mittag, Maria, Olson, Bradley J. S. C., Pangilinan, Jasmyn L., Peng, Yi, Qiu, Huan, Shu, Shengqiang, Singer, John T., Smith, Alison G., Sprecher, Brittany N., Wagner, Volker, Wang, Wenfei, Wang, Zhi-Yong, Yan, Juying, Yarish, Charles, Zäuner-Riek, Simone, Zhuang, Yunyun, Zou, Yong, Lindquist, Erika A., Grimwood, Jane, Barry, Kerrie W., Rokhsar, Daniel S., Schmutz, Jeremy, Stiller, John W., Grossman, Arthur R., & Prochnik, Simon E.. Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta). United States. doi:10.1073/pnas.1703088114.
Brawley, Susan H., Blouin, Nicolas A., Ficko-Blean, Elizabeth, Wheeler, Glen L., Lohr, Martin, Goodson, Holly V., Jenkins, Jerry W., Blaby-Haas, Crysten E., Helliwell, Katherine E., Chan, Cheong Xin, Marriage, Tara N., Bhattacharya, Debashish, Klein, Anita S., Badis, Yacine, Brodie, Juliet, Cao, Yuanyu, Collén, Jonas, Dittami, Simon M., Gachon, Claire M. M., Green, Beverley R., Karpowicz, Steven J., Kim, Jay W., Kudahl, Ulrich Johan, Lin, Senjie, Michel, Gurvan, Mittag, Maria, Olson, Bradley J. S. C., Pangilinan, Jasmyn L., Peng, Yi, Qiu, Huan, Shu, Shengqiang, Singer, John T., Smith, Alison G., Sprecher, Brittany N., Wagner, Volker, Wang, Wenfei, Wang, Zhi-Yong, Yan, Juying, Yarish, Charles, Zäuner-Riek, Simone, Zhuang, Yunyun, Zou, Yong, Lindquist, Erika A., Grimwood, Jane, Barry, Kerrie W., Rokhsar, Daniel S., Schmutz, Jeremy, Stiller, John W., Grossman, Arthur R., and Prochnik, Simon E.. 2017. "Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta)". United States. doi:10.1073/pnas.1703088114. https://www.osti.gov/servlets/purl/1376126.
@article{osti_1376126,
title = {Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta)},
author = {Brawley, Susan H. and Blouin, Nicolas A. and Ficko-Blean, Elizabeth and Wheeler, Glen L. and Lohr, Martin and Goodson, Holly V. and Jenkins, Jerry W. and Blaby-Haas, Crysten E. and Helliwell, Katherine E. and Chan, Cheong Xin and Marriage, Tara N. and Bhattacharya, Debashish and Klein, Anita S. and Badis, Yacine and Brodie, Juliet and Cao, Yuanyu and Collén, Jonas and Dittami, Simon M. and Gachon, Claire M. M. and Green, Beverley R. and Karpowicz, Steven J. and Kim, Jay W. and Kudahl, Ulrich Johan and Lin, Senjie and Michel, Gurvan and Mittag, Maria and Olson, Bradley J. S. C. and Pangilinan, Jasmyn L. and Peng, Yi and Qiu, Huan and Shu, Shengqiang and Singer, John T. and Smith, Alison G. and Sprecher, Brittany N. and Wagner, Volker and Wang, Wenfei and Wang, Zhi-Yong and Yan, Juying and Yarish, Charles and Zäuner-Riek, Simone and Zhuang, Yunyun and Zou, Yong and Lindquist, Erika A. and Grimwood, Jane and Barry, Kerrie W. and Rokhsar, Daniel S. and Schmutz, Jeremy and Stiller, John W. and Grossman, Arthur R. and Prochnik, Simon E.},
abstractNote = {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.},
doi = {10.1073/pnas.1703088114},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 31,
volume = 114,
place = {United States},
year = {2017},
month = {7}
}