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Title: The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata

Abstract

Lichens, encompassing 20,000 known species, are symbioses between specialized fungi (mycobionts), mostly ascomycetes, and unicellular green algae or cyanobacteria (photobionts). Here we describe the first parallel genomic analysis of the mycobiont Cladonia grayi and of its green algal photobiont Asterochloris glomerata. We focus on genes/predicted proteins of potential symbiotic significance, sought by surveying proteins differentially activated during early stages of mycobiont and photobiont interaction in coculture, expanded or contracted protein families, and proteins with differential rates of evolution. A) In coculture, the fungus upregulated small secreted proteins, membrane transport proteins, signal transduction components, extracellular hydrolases and, notably, a ribitol transporter and an ammonium transporter, and the alga activated DNA metabolism, signal transduction, and expression of flagellar components. B) Expanded fungal protein families include heterokaryon incompatibility proteins, polyketide synthases, and a unique set of G-protein α subunit paralogs. Expanded algal protein families include carbohydrate active enzymes and a specific subclass of cytoplasmic carbonic anhydrases. The alga also appears to have acquired by horizontal gene transfer from prokaryotes novel archaeal ATPases and Desiccation-Related Proteins. Expanded in both symbionts are signal transduction components, ankyrin domain proteins and transcription factors involved in chromatin remodeling and stress responses. The fungal transportome is contracted, as aremore » algal nitrate assimilation genes. C) In the mycobiont, slow-evolving proteins were enriched for components involved in protein translation, translocation and sorting. The surveyed genes affect stress resistance, signaling, genome reprogramming, nutritional and structural interactions. The alga carries many genes likely transferred horizontally through viruses, yet we found no evidence of inter-symbiont gene transfer. The presence in the photobiont of meiosis-specific genes supports the notion that sexual reproduction occurs in Asterochloris while they are free-living, a phenomenon with implications for the adaptability of lichens and the persistent autonomy of the symbionts. The diversity of the genes affecting the symbiosis suggests that lichens evolved by accretion of many scattered regulatory and structural changes rather than through introduction of a few key innovations. This predicts that paths to lichenization were variable in different phyla, which is consistent with the emerging consensus that ascolichens could have had a few independent origins.« less

Authors:
ORCiD logo [1];  [2];  [1];  [3];  [4];  [5];  [6];  [7];  [8];  [9];  [10];  [11];  [6];  [12];  [13];  [14];  [15];  [16];  [17];  [18] more »;  [14];  [19];  [20];  [21];  [22];  [12];  [23];  [24];  [25];  [26];  [27];  [28];  [29] « less
  1. Duke Univ., Durham, NC (United States). Dept. of Biology
  2. Duke Univ., Durham, NC (United States). Dept. of Biology; Duke Univ. Medical Center, Durham, NC (United States). Dept. of Molecular Genetics and Micorbiology
  3. Univ. of Iceland, Reykjavík (Iceland). Faculty of Life and Environmental Sciences
  4. Centre national de la recherche scientifique (CNRS), Marseille (France)
  5. Goethe Univ. Frankfurt (Germany). Molekular Biotechnologie, Fachbereich Biowissenschaftern & Buchmann Inst. for Molecular Life Sciences (BMLS)
  6. Univ. of Chicago, IL (United States). Dept. of Bioengineering; Argonne National Lab. (ANL), Argonne, IL (United States). Biosciences Division
  7. Senckenberg Biodiversity and Climate Research Center (SBiK-F), Frankfurt (Germany)
  8. Duke Univ. Medical Center, Durham, NC (United States). Dept. of Molecular Genetics and Micorbiology
  9. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States), Dept. of Plant and Microbial Biology
  10. Duke Univ., Durham, NC (United States). Dept. of Biology; Univ. of Wisconsin, Waukesha, WI (United States). College of General Studies
  11. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  12. Univ. of Iowa, Iowa City, IA (United States). Dept. of Biology
  13. Gilead Sciences, Inc., Foster City, CA (United States)
  14. Univ. de Lorraine, Champenoux (France). Interactions Arbres-Microorganismes
  15. Duke Univ., Durham, NC (United States). Dept. of Biology; North Carolina State Univ., Raleigh, NC (United States). College of Veterinary Medicine, Dept. of Population Health and Pathobiology
  16. Duke Univ., Durham, NC (United States). Dept. of Biology; St. Catherine Univ., St. Paul, MN (United States). Dept. of Biology
  17. Univ. of California, Berkeley, CA (United States), Dept. of Plant and Microbial Biology; Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology
  18. Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Microbiology and Immunology
  19. Univ. of California, Santa Barbara, CA (United States). Dept. of Ecology, Evolution, and Marine Biology
  20. Univ. of California, Los Angeles, CA (United States). Dept. of Molecular, Cell and Developmental Biology, and DOE Inst. for Genomics and Proteomics
  21. National Evolutionary Synthesis Center, Durham, NC (United States); Calico Life Sciences LLC, San Francisco, CA (United States)
  22. Univ. Nacional de Cuyo, Chacras de Coria (Argentina). Facultad de Ciencias Agrarias
  23. Senckenberg Biodiversity and Climate Research Center (SBiK-F), Frankfurt (Germany); Goethe Univ., Frankfurt (Germany). Inst. of Ecology, Evolution, and Diversity
  24. The Ohio State Univ., Columbus, OH (United States). College of Food, Agriculture, and Environmental Sciences, Dept. of Plant Pathology
  25. Univ. of Exeter (United Kingdom). College of Life & Environmental Sciences
  26. Univ. of Zurich (Switzerland). Dept. of Systematic and Evolutionary Botany
  27. Norwich Research Park (United Kingdom). The Sainsbury Lab.
  28. Univ. de Lorraine, Champenoux (France). Interactions Arbres-Microorganismes, Faculté des Sciences et Technologies
  29. Univ. of Iceland, Reykjavík (Iceland). Faculty of Life and Environmental Sciences; Univ. of Antwerp (Belgium). Vaccine & Infectious Disease Inst., Lab. of Medical Microbiology
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1572033
Grant/Contract Number:  
AC02-05CH11231; 223553; FC02-02ER63421
Resource Type:
Accepted Manuscript
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Volume: 20; Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; algal virus; coculture; fungi; gene expression; gene family evolution; horizontal gene transfer; plant-fungal interactions; symbiont autonomy; symbiosis genes

Citation Formats

Armaleo, Daniele, Müller, Olaf, Lutzoni, François, Andrésson, Ólafur S., Blanc, Guillaume, Bode, Helge B., Collart, Frank R., Dal Grande, Francesco, Dietrich, Fred, Grigoriev, Igor V., Joneson, Suzanne, Kuo, Alan, Larsen, Peter E., Logsdon, John M., Lopez, David, Martin, Francis, May, Susan P., McDonald, Tami R., Merchant, Sabeeha S., Miao, Vivian, Morin, Emmanuelle, Oono, Ryoko, Pellegrini, Matteo, Rubinstein, Nimrod, Sanchez-Puerta, Maria Virginia, Savelkoul, Elizabeth, Schmitt, Imke, Slot, Jason C., Soanes, Darren, Szövényi, Péter, Talbot, Nicholas J., Veneault-Fourrey, Claire, and Xavier, Basil B. The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata. United States: N. p., 2019. Web. doi:10.1186/s12864-019-5629-x.
Armaleo, Daniele, Müller, Olaf, Lutzoni, François, Andrésson, Ólafur S., Blanc, Guillaume, Bode, Helge B., Collart, Frank R., Dal Grande, Francesco, Dietrich, Fred, Grigoriev, Igor V., Joneson, Suzanne, Kuo, Alan, Larsen, Peter E., Logsdon, John M., Lopez, David, Martin, Francis, May, Susan P., McDonald, Tami R., Merchant, Sabeeha S., Miao, Vivian, Morin, Emmanuelle, Oono, Ryoko, Pellegrini, Matteo, Rubinstein, Nimrod, Sanchez-Puerta, Maria Virginia, Savelkoul, Elizabeth, Schmitt, Imke, Slot, Jason C., Soanes, Darren, Szövényi, Péter, Talbot, Nicholas J., Veneault-Fourrey, Claire, & Xavier, Basil B. The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata. United States. doi:10.1186/s12864-019-5629-x.
Armaleo, Daniele, Müller, Olaf, Lutzoni, François, Andrésson, Ólafur S., Blanc, Guillaume, Bode, Helge B., Collart, Frank R., Dal Grande, Francesco, Dietrich, Fred, Grigoriev, Igor V., Joneson, Suzanne, Kuo, Alan, Larsen, Peter E., Logsdon, John M., Lopez, David, Martin, Francis, May, Susan P., McDonald, Tami R., Merchant, Sabeeha S., Miao, Vivian, Morin, Emmanuelle, Oono, Ryoko, Pellegrini, Matteo, Rubinstein, Nimrod, Sanchez-Puerta, Maria Virginia, Savelkoul, Elizabeth, Schmitt, Imke, Slot, Jason C., Soanes, Darren, Szövényi, Péter, Talbot, Nicholas J., Veneault-Fourrey, Claire, and Xavier, Basil B. Tue . "The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata". United States. doi:10.1186/s12864-019-5629-x. https://www.osti.gov/servlets/purl/1572033.
@article{osti_1572033,
title = {The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata},
author = {Armaleo, Daniele and Müller, Olaf and Lutzoni, François and Andrésson, Ólafur S. and Blanc, Guillaume and Bode, Helge B. and Collart, Frank R. and Dal Grande, Francesco and Dietrich, Fred and Grigoriev, Igor V. and Joneson, Suzanne and Kuo, Alan and Larsen, Peter E. and Logsdon, John M. and Lopez, David and Martin, Francis and May, Susan P. and McDonald, Tami R. and Merchant, Sabeeha S. and Miao, Vivian and Morin, Emmanuelle and Oono, Ryoko and Pellegrini, Matteo and Rubinstein, Nimrod and Sanchez-Puerta, Maria Virginia and Savelkoul, Elizabeth and Schmitt, Imke and Slot, Jason C. and Soanes, Darren and Szövényi, Péter and Talbot, Nicholas J. and Veneault-Fourrey, Claire and Xavier, Basil B.},
abstractNote = {Lichens, encompassing 20,000 known species, are symbioses between specialized fungi (mycobionts), mostly ascomycetes, and unicellular green algae or cyanobacteria (photobionts). Here we describe the first parallel genomic analysis of the mycobiont Cladonia grayi and of its green algal photobiont Asterochloris glomerata. We focus on genes/predicted proteins of potential symbiotic significance, sought by surveying proteins differentially activated during early stages of mycobiont and photobiont interaction in coculture, expanded or contracted protein families, and proteins with differential rates of evolution. A) In coculture, the fungus upregulated small secreted proteins, membrane transport proteins, signal transduction components, extracellular hydrolases and, notably, a ribitol transporter and an ammonium transporter, and the alga activated DNA metabolism, signal transduction, and expression of flagellar components. B) Expanded fungal protein families include heterokaryon incompatibility proteins, polyketide synthases, and a unique set of G-protein α subunit paralogs. Expanded algal protein families include carbohydrate active enzymes and a specific subclass of cytoplasmic carbonic anhydrases. The alga also appears to have acquired by horizontal gene transfer from prokaryotes novel archaeal ATPases and Desiccation-Related Proteins. Expanded in both symbionts are signal transduction components, ankyrin domain proteins and transcription factors involved in chromatin remodeling and stress responses. The fungal transportome is contracted, as are algal nitrate assimilation genes. C) In the mycobiont, slow-evolving proteins were enriched for components involved in protein translation, translocation and sorting. The surveyed genes affect stress resistance, signaling, genome reprogramming, nutritional and structural interactions. The alga carries many genes likely transferred horizontally through viruses, yet we found no evidence of inter-symbiont gene transfer. The presence in the photobiont of meiosis-specific genes supports the notion that sexual reproduction occurs in Asterochloris while they are free-living, a phenomenon with implications for the adaptability of lichens and the persistent autonomy of the symbionts. The diversity of the genes affecting the symbiosis suggests that lichens evolved by accretion of many scattered regulatory and structural changes rather than through introduction of a few key innovations. This predicts that paths to lichenization were variable in different phyla, which is consistent with the emerging consensus that ascolichens could have had a few independent origins.},
doi = {10.1186/s12864-019-5629-x},
journal = {BMC Genomics},
number = 1,
volume = 20,
place = {United States},
year = {2019},
month = {7}
}

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journal, April 2007

  • Emanuelsson, Olof; Brunak, Søren; von Heijne, Gunnar
  • Nature Protocols, Vol. 2, Issue 4
  • DOI: 10.1038/nprot.2007.131

The Genomics of Obligate (and Nonobligate) Biotrophs
journal, September 2012


Genome-Wide Phylogenetic Comparative Analysis of Plant Transcriptional Regulation: A Timeline of Loss, Gain, Expansion, and Correlation with Complexity
journal, January 2010

  • Lang, Daniel; Weiche, Benjamin; Timmerhaus, Gerrit
  • Genome Biology and Evolution, Vol. 2
  • DOI: 10.1093/gbe/evq032

RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006


Velvet: Algorithms for de novo short read assembly using de Bruijn graphs
journal, February 2008


Assessing the gene space in draft genomes
journal, November 2008

  • Parra, Genis; Bradnam, Keith; Ning, Zemin
  • Nucleic Acids Research, Vol. 37, Issue 1
  • DOI: 10.1093/nar/gkn916

Using a meiosis detection toolkit to investigate ancient asexual “scandals” and the evolution of sex
journal, January 2008

  • Schurko, Andrew M.; Logsdon, John M.
  • BioEssays, Vol. 30, Issue 6
  • DOI: 10.1002/bies.20764

Two Meiotic Crossover Classes Cohabit in Arabidopsis
journal, April 2005


trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009


Cohesin gene defects may impair sister chromatid alignment and genome stability in Arabidopsis thaliana
journal, June 2009