Evolution of zygomycete secretomes and the origins of terrestrial fungal ecologies

Chang, Ying; Wang, Yan; Mondo, Stephen; Ahrendt, Steven; Andreopoulos, William; Barry, Kerrie; Beard, Jeff; Benny, Gerald L.; Blankenship, Sabrina; Bonito, Gregory; Cuomo, Christina; Desiro, Alessandro; Gervers, Kyle A.; Hundley, Hope; Kuo, Alan; LaButti, Kurt; Lang, B. Franz; Lipzen, Anna; O’Donnell, Kerry; Pangilinan, Jasmyn; Reynolds, Nicole; Sandor, Laura; Smith, Matthew E.; Tsang, Adrian; Grigoriev, Igor V.; Stajich, Jason E.; Spatafora, Joseph W.

doi:10.1016/j.isci.2022.104840

Title: Evolution of zygomycete secretomes and the origins of terrestrial fungal ecologies

Journal Article · 02 August 2022 · iScience

DOI: https://doi.org/10.1016/j.isci.2022.104840 · OSTI ID:1907592

^[1]; Wang, Yan ^[2]; Mondo, Stephen ^[3]; Ahrendt, Steven ^[3]; Andreopoulos, William ^[3]; Barry, Kerrie ^[3]; Beard, Jeff ^[4]; Benny, Gerald L. ^[5]; Blankenship, Sabrina ^[4]; Bonito, Gregory ^[6]; Cuomo, Christina ^[7]; Desiro, Alessandro ^[6]; Gervers, Kyle A. ^[4]; Hundley, Hope ^[3]; Kuo, Alan ^[3]; LaButti, Kurt ^[3]; Lang, B. Franz ^[8]; Lipzen, Anna ^[3]; O’Donnell, Kerry ^[9]; Pangilinan, Jasmyn ^[3] more »

Oregon State University, Corvallis, OR (United States); Yale-NUS College (Singapore)
University of California, Riverside, CA (United States); University of Toronto Scarborough (Canada)
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
Oregon State University, Corvallis, OR (United States)
University of Florida, Gainesville, FL (United States)
Michigan State University, East Lansing, MI (United States)
Massachusetts Institute of Technology (MIT), Cambridge, MA (United States); Harvard University, Cambridge, MA (United States)
University of Montreal, QC (Canada)
US Department of Agriculture (USDA), Peoria, IL (United States)
Concordia University, Montreal (Canada)
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); University of California, Berkeley, CA (United States)
University of California, Riverside, CA (United States)

Fungi survive in diverse ecological niches by secreting proteins and other molecules into the environment to acquire food and interact with various biotic and abiotic stressors. Fungal secretome content is, therefore, believed to be tightly linked to fungal ecologies. We sampled 132 genomes from the early-diverging terrestrial fungal lineage zygomycetes (Mucoromycota and Zoopagomycota) and characterized their secretome composition. Our analyses revealed that phylogeny played an important role in shaping the secretome composition of zygomycete fungi with trophic mode contributing a smaller amount. Reconstruction of the evolution of secreted digestive enzymes revealed lineage-specific expansions, indicating that Mucoromycota and Zoopagomycota followed different trajectories early in their evolutionary history. We identified the presence of multiple pathogenicity-related proteins in the lineages known as saprotrophs, suggesting that either the ecologies of these fungi are incompletely known, and/or that these pathogenicity-related proteins have important functions associated with saprotrophic ecologies, both of which invite further investigation.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: National Institutes of Health (NIH); National Science Foundation (NSF); USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1907592

Journal Information:: iScience, Journal Name: iScience Journal Issue: 8 Vol. 25; ISSN 2589-0042

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (56)

Prediction of GPI-anchored proteins with pointer neural networks Gíslason, Magnús Halldór; Nielsen, Henrik; Almagro Armenteros, José Juan Current Research in Biotechnology, Vol. 3 https://doi.org/10.1016/j.crbiot.2021.01.001	journal	January 2021
A genome-scale phylogeny of the kingdom Fungi Li, Yuanning; Steenwyk, Jacob L.; Chang, Ying Current Biology, Vol. 31, Issue 8 https://doi.org/10.1016/j.cub.2021.01.074	journal	April 2021
FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild Nguyen, Nhu H.; Song, Zewei; Bates, Scott T. Fungal Ecology, Vol. 20 https://doi.org/10.1016/j.funeco.2015.06.006	journal	April 2016
Comparative analysis of secretomes in basidiomycete fungi Alfaro, Manuel; Oguiza, José A.; Ramírez, Lucía Journal of Proteomics, Vol. 102 https://doi.org/10.1016/j.jprot.2014.03.001	journal	May 2014
Reconsidering mutualistic plant–fungal interactions through the lens of effector biology Plett, Jonathan M.; Martin, Francis Current Opinion in Plant Biology, Vol. 26 https://doi.org/10.1016/j.pbi.2015.06.001	journal	August 2015
Full-length transcriptome assembly from RNA-Seq data without a reference genome Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran Nature Biotechnology, Vol. 29, Issue 7 https://doi.org/10.1038/nbt.1883	journal	May 2011
Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data Chin, Chen-Shan; Alexander, David H.; Marks, Patrick Nature Methods, Vol. 10, Issue 6 https://doi.org/10.1038/nmeth.2474	journal	May 2013
Fast and sensitive protein alignment using DIAMOND Buchfink, Benjamin; Xie, Chao; Huson, Daniel H. Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3176	journal	November 2014
Phased diploid genome assembly with single-molecule real-time sequencing Chin, Chen-Shan; Peluso, Paul; Sedlazeck, Fritz J. Nature Methods, Vol. 13, Issue 12 https://doi.org/10.1038/nmeth.4035	journal	October 2016
Comparative genomics reveals the origin of fungal hyphae and multicellularity Kiss, Enikő; Hegedüs, Botond; Virágh, Máté Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12085-w	journal	September 2019
Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits Miyauchi, Shingo; Kiss, Enikő; Kuo, Alan Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-18795-w	journal	October 2020
Genome-scale phylogenetic analyses confirm Olpidium as the closest living zoosporic fungus to the non-flagellated, terrestrial fungi Chang, Ying; Rochon, D’Ann; Sekimoto, Satoshi Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-82607-4	journal	February 2021
High-quality draft assemblies of mammalian genomes from massively parallel sequence data Gnerre, S.; MacCallum, I.; Przybylski, D. Proceedings of the National Academy of Sciences, Vol. 108, Issue 4 https://doi.org/10.1073/pnas.1017351108	journal	December 2010
Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis Tisserant, E.; Malbreil, M.; Kuo, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 50 https://doi.org/10.1073/pnas.1313452110	journal	November 2013
Structural base for the transfer of GPI-anchored glycoproteins into fungal cell walls Vogt, Marian Samuel; Schmitz, Gesa Felicitas; Varón Silva, Daniel Proceedings of the National Academy of Sciences, Vol. 117, Issue 36 https://doi.org/10.1073/pnas.2010661117	journal	August 2020
Inferring duplications, losses, transfers and incomplete lineage sorting with nonbinary species trees Stolzer, Maureen; Lai, Han; Xu, Minli Bioinformatics, Vol. 28, Issue 18 https://doi.org/10.1093/bioinformatics/bts386	journal	September 2012
InterProScan 5: genome-scale protein function classification Jones, P.; Binns, D.; Chang, H. -Y. Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu031	journal	January 2014
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
FinisherSC: a repeat-aware tool for upgrading de novo assembly using long reads Lam, Ka-Kit; LaButti, Kurt; Khalak, Asif Bioinformatics, Vol. 31, Issue 19 https://doi.org/10.1093/bioinformatics/btv280	journal	June 2015
ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R Paradis, Emmanuel; Schliep, Klaus Bioinformatics, Vol. 35, Issue 3 https://doi.org/10.1093/bioinformatics/bty633	journal	July 2018
Ultra-low input transcriptomics reveal the spore functional content and phylogenetic affiliations of poorly studied arbuscular mycorrhizal fungi Beaudet, Denis; Chen, Eric C. H.; Mathieu, Stephanie DNA Research, Vol. 25, Issue 2 https://doi.org/10.1093/dnares/dsx051	journal	December 2017
In Silico Characterization and Molecular Evolutionary Analysis of a Novel Superfamily of Fungal Effector Proteins Stergiopoulos, Ioannis; Kourmpetis, Yiannis A. I.; Slot, Jason C. Molecular Biology and Evolution, Vol. 29, Issue 11 https://doi.org/10.1093/molbev/mss143	journal	July 2012
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
dbCAN: a web resource for automated carbohydrate-active enzyme annotation Yin, Yanbin; Mao, Xizeng; Yang, Jincai Nucleic Acids Research, Vol. 40, Issue W1 https://doi.org/10.1093/nar/gks479	journal	May 2012
MycoCosm portal: gearing up for 1000 fungal genomes Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1183	journal	December 2013
The MEROPS database of proteolytic enzymes, their substrates and inhibitors in 2017 and a comparison with peptidases in the PANTHER database Rawlings, Neil D.; Barrett, Alan J.; Thomas, Paul D. Nucleic Acids Research, Vol. 46, Issue D1 https://doi.org/10.1093/nar/gkx1134	journal	November 2017
Velvet: Algorithms for de novo short read assembly using de Bruijn graphs Zerbino, D. R.; Birney, E. Genome Research, Vol. 18, Issue 5 https://doi.org/10.1101/gr.074492.107	journal	February 2008
Whole-Genome Sequence Assembly for Mammalian Genomes: Arachne 2 Jaffe, D. B. Genome Research, Vol. 13, Issue 1 https://doi.org/10.1101/gr.828403	journal	January 2003
The β‐1,3‐glucanosyltransferases (Gels) affect the structure of the rice blast fungal cell wall during appressorium‐mediated plant infection Samalova, Marketa; Mélida, Hugo; Vilaplana, Francisco Cellular Microbiology, Vol. 19, Issue 3 https://doi.org/10.1111/cmi.12659	journal	October 2016
Improved prediction of fungal effector proteins from secretomes with EffectorP 2.0: Prediction of fungal effectors with EffectorP 2.0 Sperschneider, Jana; Dodds, Peter N.; Gardiner, Donald M. Molecular Plant Pathology, Vol. 19, Issue 9 https://doi.org/10.1111/mpp.12682	journal	May 2018
Phylogenomics of Endogonaceae and evolution of mycorrhizas within Mucoromycota Chang, Ying; Desirò, Alessandro; Na, Hyunsoo New Phytologist, Vol. 222, Issue 1 https://doi.org/10.1111/nph.15613	journal	January 2019
Humidity and high temperature are important for predicting fungal disease outbreaks worldwide Romero, Ferran; Cazzato, Sabrina; Walder, Florian New Phytologist, Vol. 234, Issue 5 https://doi.org/10.1111/nph.17340	journal	April 2021
The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes Floudas, Dimitrios; Binder, Manfred; Riley, Robert Science, Vol. 336, Issue 6089 https://doi.org/10.1126/science.1221748	journal	June 2012
Human Pathogenic Entomophthorales Vilela, Raquel; Mendoza, Leonel Clinical Microbiology Reviews, Vol. 31, Issue 4 https://doi.org/10.1128/CMR.00014-18	journal	August 2018
Comparative Genomics Reveals the Core Gene Toolbox for the Fungus-Insect Symbiosis Wang, Yan; Stata, Matt; Wang, Wei mBio, Vol. 9, Issue 3 https://doi.org/10.1128/mBio.00636-18	journal	May 2018
The Fungal Cell Wall: Structure, Biosynthesis, and Function Gow, Neil A. R.; Latge, Jean-Paul; Munro, Carol A. Microbiology Spectrum, Vol. 5, Issue 3 https://doi.org/10.1128/microbiolspec.FUNK-0035-2016	journal	June 2017
Fungal Effectors and Plant Susceptibility Lo Presti, Libera; Lanver, Daniel; Schweizer, Gabriel Annual Review of Plant Biology, Vol. 66, Issue 1 https://doi.org/10.1146/annurev-arplant-043014-114623	journal	April 2015
Compositions of fungal secretomes indicate a greater impact of phylogenetic history than lifestyle adaptation Krijger, Jorrit-Jan; Thon, Michael R.; Deising, Holger B. BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-722	journal	January 2014
The effector candidate repertoire of the arbuscular mycorrhizal fungus Rhizophagus clarus Sędzielewska Toro, Kinga; Brachmann, Andreas BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-2422-y	journal	February 2016
OrthoFinder: phylogenetic orthology inference for comparative genomics Emms, David M.; Kelly, Steven Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-019-1832-y	journal	November 2019
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
Expanding the Paradigms of Plant Pathogen Life History and Evolution of Parasitic Fitness beyond Agricultural Boundaries Morris, Cindy E.; Bardin, Marc; Kinkel, Linda L. PLoS Pathogens, Vol. 5, Issue 12 https://doi.org/10.1371/journal.ppat.1000693	journal	December 2009
Indifferent, Affectionate, or Deceitful: Lifestyles and Secretomes of Fungi Lowe, Rohan G. T.; Howlett, Barbara J. PLoS Pathogens, Vol. 8, Issue 3 https://doi.org/10.1371/journal.ppat.1002515	journal	March 2012
LysM Effectors: Secreted Proteins Supporting Fungal Life Kombrink, Anja; Thomma, Bart P. H. J. PLoS Pathogens, Vol. 9, Issue 12 https://doi.org/10.1371/journal.ppat.1003769	journal	December 2013
Hijacked: Co-option of host behavior by entomophthoralean fungi Gryganskyi, Andrii P.; Mullens, Bradley A.; Gajdeczka, Michael T. PLOS Pathogens, Vol. 13, Issue 5 https://doi.org/10.1371/journal.ppat.1006274	journal	May 2017
Molecular mechanisms of mucormycosis—The bitter and the sweet Baldin, Clara; Ibrahim, Ashraf S. PLOS Pathogens, Vol. 13, Issue 8 https://doi.org/10.1371/journal.ppat.1006408	journal	August 2017
Associations between species and groups of sites: indices and statistical inference Cáceres, Miquel De; Legendre, Pierre Ecology, Vol. 90, Issue 12 https://doi.org/10.1890/08-1823.1	journal	December 2009
Multiple Regression and Correlation Extensions of the Mantel Test of Matrix Correspondence Smouse, Peter E.; Long, Jeffrey C.; Sokal, Robert R. Systematic Zoology, Vol. 35, Issue 4 https://doi.org/10.2307/2413122	journal	December 1986
The Fungal Cell Wall: Candida, Cryptococcus, and Aspergillus Species Garcia-Rubio, Rocio; de Oliveira, Haroldo C.; Rivera, Johanna Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02993	journal	January 2020
Seeking the Roles for Fungal Small-Secreted Proteins in Affecting Saprophytic Lifestyles Feldman, Daria; Yarden, Oded; Hadar, Yitzhak Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.00455	journal	March 2020
LysM Proteins Regulate Fungal Development and Contribute to Hyphal Protection and Biocontrol Traits in Clonostachys rosea Dubey, Mukesh; Vélëz, Heriberto; Broberg, Martin Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.00679	journal	April 2020
Kingdom-Wide Analysis of Fungal Small Secreted Proteins (SSPs) Reveals their Potential Role in Host Association Kim, Ki-Tae; Jeon, Jongbum; Choi, Jaeyoung Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00186	journal	February 2016
The Comparison of Expressed Candidate Secreted Proteins from Two Arbuscular Mycorrhizal Fungi Unravels Common and Specific Molecular Tools to Invade Different Host Plants Kamel, Laurent; Tang, Nianwu; Malbreil, Mathilde Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00124	journal	February 2017
Fascinating Fasciclins: A Surprisingly Widespread Family of Proteins that Mediate Interactions between the Cell Exterior and the Cell Surface Seifert, Georg International Journal of Molecular Sciences, Vol. 19, Issue 6 https://doi.org/10.3390/ijms19061628	journal	May 2018
Lysin Motif (LysM) Proteins: Interlinking Manipulation of Plant Immunity and Fungi Hu, Shu-Ping; Li, Jun-Jiao; Dhar, Nikhilesh International Journal of Molecular Sciences, Vol. 22, Issue 6 https://doi.org/10.3390/ijms22063114	journal	March 2021
A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data Spatafora, Joseph W.; Chang, Ying; Benny, Gerald L. Mycologia, Vol. 108, Issue 5 https://doi.org/10.3852/16-042	journal	September 2016

Similar Records

Divergent Evolution of Early Terrestrial Fungi Reveals the Evolution of Mucormycosis Pathogenicity Factors

Journal Article · 2023 · Genome Biology and Evolution · OSTI ID:1968629

Wang, Yan; Chang, Ying; Ortañez, Jericho; +20 more

Sequencing the Genomes of the First Terrestrial Fungal Lineages: What Have We Learned?

Journal Article · 2023 · Microorganisms · OSTI ID:2242458

Gryganskyi, Andrii P.; Golan, Jacob; Muszewska, Anna; +24 more

Comparative analysis of secretomes from Ectomycorrhizal fungi with an emphasis on small-secreted proteins

Journal Article · 2015 · Frontiers in Microbiology · OSTI ID:1241128

Pellegrin, Clement; Morin, Emmanuelle; Martin, Francis M.; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Evolution of zygomycete secretomes and the origins of terrestrial fungal ecologies

Citation Formats

References (56)

Similar Records

Related Subjects