Open Access
In silico analysis of the expression profile of AA9 Lytic Polysaccharide Monooxygenases (LPMOs) and the CDH Cellobiose Dehydrogenase enzyme in wood-degrader Agaricomycetes. The Pleurotus ostreatus case
(Elsevier, 2024-08-22) Jiménez Miguel, Idoia; Roscales, Gabriel; Garde Sagardoy, Edurne; Chuina Tomazeli, Emilia; Honda, Yoichi; Lipzen, Anna; Lail, Kathleen; Bauer, Diane; Barry, Kerrie; Grigoriev, Igor V.; Ramírez L.; Ramírez Nasto, Lucía; Institute for Multidisciplinary Research in Applied Biology - IMAB; Universidad Pública de Navarra / Nafarroako Unibertsitate Publikoa
Lignocellulose, the Earth's most abundant biopolymer, is degraded by wood-decaying fungi, specifically white rot fungi (WRF) and brown rot fungi (BRF), which use different strategies. This study examines the expression profiles of the AA9 and CDH enzymes of three WRF species (Heterobasidion annosum, Phanerochaete chrysosporium, and Pleurotus ostreatus) and two BRF species (Fomitopsis pinicola and Rhodonia placenta) from the Agaricomycetes class, grown on poplar wood or glucose as the sole carbon source. Mycelia were collected between days 10 and 12, revealing distinct lignocellulose degradation strategies between WRF and BRF, evidenced by the upregulation of AA9 LPMO (lytic polysaccharide monooxygenases) and AA3_1 (Cellobiose Dehydrogenase) genes, with the co-occurrence of both types of transcripts at the time of mycelial collection. The genome analysis showed variability in the number of AA9LPMO genes between WRF and BRF, which were differentially regulated depending on the carbon source. WRF exhibited a significant upregulation of AA9 LPMO genes,. In Phanerochaete chrysosporium, only one AA9LPMO gene was homologous to Pleurotus ostreatus, which had the highest number of AA9LPMO genes among the WRF studied. Some AA9 LPMO genes in Pleurotus ostreatus were associated to transposable elements (TEs, mainly footprints of LTRs) and grouped in clustered. LTRs were found either in the flanking or within the gene coding regions with no effect on gene transcription. In silico analysis of the AA9LPMO proteins in WRF uncovered distinct features at their C-terminal ends. Most of them lacked an appended module, but those with a CBM1 were highly induced in poplar wood media. The proportion of AA9 proteins with a CBM1 module was similar in Phanerochaete chrysosporium and Heterobasidion irregulare, but lower in Pleurotus ostreatus, which contained more AA9LPMO genes overall. In Pleurotus ostreatus, AA9LPMO proteins were grouped into three clades based on their C oxidizing type, with each clade containing proteins with specific features. The abundance (redundancy) of AA9LPMO genes in WRF especially associated to footprints LTRs in Pleurotus ostreatus suggests these genes may have other roles beyond lignocellulose degradation.
Open Access
Metatranscriptomics sheds light on the links between the functional traits of fungal guilds and ecological processes in forest soil ecosystems
(Blackwell Scientific Publications Ltd, 2023) Auer, Lucas; Buée, Marc; Fauchery, Laure; Lombard, Vincent; Barry, Kerrie; Clum, Alicia; Copeland, Alex; Daum, Chris; LaButti, Kurt; Singan, Vasanth; Yoshinaga, Yuko; Martineau, Christine; Castillo Martínez, Federico; Alfaro Sánchez, Manuel; Imbert Rodríguez, Bosco; Ramírez Nasto, Lucía; Castanera Andrés, Raúl; Pisabarro de Lucas, Gerardo; Finlay, Roger; Lindahl, Björn D.; Olson, Ake; Séguin, Armand; Kohler, Annegret; Henrissat, Bernard; Grigoriev, Igor V.; Martin, Francis; Agronomía, Biotecnología y Alimentación; Agronomia, Bioteknologia eta Elikadura; Institute for Multidisciplinary Research in Applied Biology - IMAB
Soil fungi belonging to different functional guilds, such as saprotrophs, pathogens, and mycorrhizal symbionts, play key roles in forest ecosystems. To date, no study has compared the actual gene expression of these guilds in different forest soils. We used metatranscriptomics to study the competition for organic resources by these fungal groups in boreal, temperate, and Mediterranean forest soils. Using a dedicated mRNA annotation pipeline combined with the JGI MycoCosm database, we compared the transcripts of these three fungal guilds, targeting enzymes involved in C- and N mobilization from plant and microbial cell walls. Genes encoding enzymes involved in the degradation of plant cell walls were expressed at a higher level in saprotrophic fungi than in ectomycorrhizal and pathogenic fungi. However, ectomycorrhizal and saprotrophic fungi showed similarly high expression levels of genes encoding enzymes involved in fungal cell wall degradation. Transcripts for N-related transporters were more highly expressed in ectomycorrhizal fungi than in other groups. We showed that ectomycorrhizal and saprotrophic fungi compete for N in soil organic matter, suggesting that their interactions could decelerate C cycling. Metatranscriptomics provides a unique tool to test controversial ecological hypotheses and to better understand the underlying ecological processes involved in soil functioning and carbon stabilization.
Open Access
Expansion of the global RNA virome reveals diverse clades of bacteriophages
(Elsevier, 2022) Neri, Uri; Wolf, Yuri I.; Roux, Simon; Camargo, Antonio Pedro; Lee, Benjamin; Kazlauskas, Darius; Chen, I. Min; Ivanova, Natalia; Zeigler Allen, Lisa; Paez-Espino, David; Bryant, Donald A.; Bhaya, Devaki; Krupovic, Mart; Dolja, Valerian V.; Kyrpides, Nikos C.; Koonin, Eugene V.; Gophna, Uri; RNA Virus Discovery Consortium; Narrowe, Adrienne B.; Ramírez Nasto, Lucía; Wang, Zhong; Nusslein, Klaus; Meredith, Laura K.; Buée, Marc; Huntemann, Marcel; Kalyuzhnaya, Marina G.; Waldrop, Mark P.; Sullivan, Matthew B.; Schrenk, Matthew O.; Hess, Matthias; Vega, Michael A.; O’Malley, Michelle A.; Medina, Mónica; Gilbert, Naomi E.; Delherbe, Nathalie; Mason, Olivia U.; Probst, Alexander J.; Sczyrba, Alexander; Kohler, Annegret; Séguin, Armand; Shade, Ashley; Campbell, Barbara J.; Lindahl, Björn D.; Reese, Brandi Kiel; Roque, Breanna M.; DeRito, Christopher; Averill, Colin; Cullen, Daniel; Beck, David A.C.; Walsh, David A.; Ward, David M.; Wu, Dongying; Eloe-Fadrosh, Emiley; Brodie, Eoin L.; Dijkstra, Paul; Chuckran, Peter F.; Baldrian, Petr; Constant, Philippe; Stepanauskas, Ramunas; Daly, Rebecca A.; Lamendella, Regina; Gruninger, Robert J.; McKay, Robert M.; Hylander, Samuel; Lebeis, Sarah L.; Esser, Sarah P.; Acinas, Silvia G.; Young, Erica B.; Lilleskov, Erik A.; Castillo, Federico J.; Martin, Francis; LeCleir, Gary R.; Attwood, Graeme T.; Cadillo-Quiroz, Hinsby; Simon, Holly M.; Hewson, Ian; Grigoriev, Igor V.; Tiedje, James M.; Jansson, Janet K.; Lee, Janey; VanderGheynst, Jean S.; Dangl, Jeff; Bowman, Jeff S.; Blanchard, Jeffrey L.; Bowen, Jennifer L.; Xu, Jiangbing; Banfield, Jillian F.; Deming, Jody W.; Kostka, Joel E.; Gladden, John M.; Rapp, Josephine Z.; Sharpe, Joshua; McMahon, Katherine D.; Treseder, Kathleen K.; Bidle, Kay D.; Wrighton, Kelly C.; Thamatrakoln, Kimberlee; Wilhelm, Steven S.; Singer, Steven W.; Tringe, Susannah S.; Woyke, Tanja; Reddy, T.B.K.; Bell, Terrence H.; Mock, Thomas; McAllister, Tim; Thiel, Vera; Denef, Vincent J.; Liu, Wen-Tso; Martens-Habbena, Willm; Liu, Xiao-Jun Allen; Cooper, Zachary S.; Agronomía, Biotecnología y Alimentación; Agronomia, Bioteknologia eta Elikadura; Institute for Multidisciplinary Research in Applied Biology - IMAB
High-throughput RNA sequencing offers broad opportunities to explore the Earth RNA virome. Mining 5,150 diverse metatranscriptomes uncovered >2.5 million RNA virus contigs. Analysis of >330,000 RNA-dependent RNA polymerases (RdRPs) shows that this expansion corresponds to a 5-fold increase of the known RNA virus diversity. Gene content analysis revealed multiple protein domains previously not found in RNA viruses and implicated in virus-host interactions. Extended RdRP phylogeny supports the monophyly of the five established phyla and reveals two putative additional bacteriophage phyla and numerous putative additional classes and orders. The dramatically expanded phylum Lenarviricota, consisting of bacterial and related eukaryotic viruses, now accounts for a third of the RNA virome. Identification of CRISPR spacer matches and bacteriolytic proteins suggests that subsets of picobirnaviruses and partitiviruses, previously associated with eukaryotes, infect prokaryotic hosts.
Open Access
Genomic analysis enlightens agaricales lifestyle evolution and increasing peroxidase diversity
(Oxford University Press, 2021) Ruiz Dueñas, Francisco J.; Barrasa, José M.; Sánchez-García, Marisol; Camarero, Susana; Miyauchi, Shingo; Linde, Dolores; Babiker, Rashid; Drula, Elodie; Ayuso-Fernández, Iván; Pacheco, Remedios; Padilla, Guillermo; Ferreira, Patricia; Barriuso, Jorge; Kellner, Harald; Castanera Andrés, Raúl; Alfaro Sánchez, Manuel; Ramírez Nasto, Lucía; Pisabarro de Lucas, Gerardo; Riley, Robert; Kuo, Alan; Andreopoulos, William; LaButti, Kurt; Pangilinan, Jasmyn; Tritt, Andrew; Lipzen, Anna; He, Guifen; Yan, Mi; Vivian, Ng; Grigoriev, Igor V.; Cullen, Daniel; Martin, Francis; Rosso, Marie-Noëlle; Henrissat, Bernard; Hibbett, David; Martínez, Ángel T.; Institute for Multidisciplinary Research in Applied Biology - IMAB
As actors of global carbon cycle, Agaricomycetes (Basidiomycota) have developed complex enzymatic machineries that allow them to decompose all plant polymers, including lignin. Among them, saprotrophic Agaricales are characterized by an unparalleled diversity of habitats and lifestyles. Comparative analysis of 52 Agaricomycetes genomes (14 of them sequenced de novo) reveals that Agaricales possess a large diversity of hydrolytic and oxidative enzymes for lignocellulose decay. Based on the gene families with the predicted highest evolutionary rates-namely cellulose-binding CBM1, glycoside hydrolase GH43, lytic polysaccharide monooxygenase AA9, class-II peroxidases, glucose-methanol-choline oxidase/dehydrogenases, laccases, and unspecific peroxygenases-we reconstructed the lifestyles of the ancestors that led to the extant lignocellulose-decomposing Agaricomycetes. The changes in the enzymatic toolkit of ancestral Agaricales are correlated with the evolution of their ability to grow not only on wood but also on leaf litter and decayed wood, with grass-litter decomposers as the most recent eco-physiological group. In this context, the above families were analyzed in detail in connection with lifestyle diversity. Peroxidases appear as a central component of the enzymatic toolkit of saprotrophic Agaricomycetes, consistent with their essential role in lignin degradation and high evolutionary rates. This includes not only expansions/losses in peroxidase genes common to other basidiomycetes but also the widespread presence in Agaricales (and Russulales) of new peroxidases types not found in wood-rotting Polyporales, and other Agaricomycetes orders. Therefore, we analyzed the peroxidase evolution in Agaricomycetes by ancestralsequence reconstruction revealing several major evolutionary pathways and mapped the appearance of the different enzyme types in a time-calibrated species tree.

Ramírez Nasto, Lucía

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