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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; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; more »; ; ; ; ; ; ; ; ; ; ; ; ; « less
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)
OSTI Identifier:
1618576
Alternate Identifier(s):
OSTI ID: 1572033
Grant/Contract Number:  
FWP 61327; AC02-05CH11231; FC02-02ER63421; 112442; 223553
Resource Type:
Published Article
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Name: BMC Genomics Journal Volume: 20 Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer Science + Business Media
Country of Publication:
United Kingdom
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, Jr, 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 Kingdom: N. p., 2019. Web. https://doi.org/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, Jr, 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 Kingdom. https://doi.org/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, Jr, 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 Kingdom. https://doi.org/10.1186/s12864-019-5629-x.
@article{osti_1618576,
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, Jr, 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 Kingdom},
year = {2019},
month = {7}
}

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