Rosa Milagros Corrales, Jeremy Vincent, Lucien Crobu, Rachel Neish, Binita Nepal, Julien Espeut, Grégoire Pasquier, Ghislain Gillard, Chantal Cazevieille, Jeremy C. Mottram, Dawn M. Wetzel, Yvon Sterkers, Krzysztof Rogowski, Maude F. Lévêque
Tubulin detyrosination has been implicated in various human disorders and is important for regulating microtubule dynamics. While in most organisms this modification is restricted to α-tubulin, in trypanosomatid parasites, it occurs on both α- and β-tubulin. Here, we show that in Leishmania , a single vasohibin (LmVASH) enzyme is responsible for differential kinetics of α- and β-tubulin detyrosination. LmVASH knockout parasites, which are completely devoid of detyrosination, show decreased levels of glutamylation and exhibit a strongly diminished pathogenicity in mice, correlating with decreased proliferation in macrophages. Reduced virulence is associated with altered morphogenesis and flagellum remodeling in detyrosination-deficient amastigotes. Flagellum shortening in the absence of detyrosination is caused by hyperactivity of a microtubule-depolymerizing Kinesin-13 homolog, demonstrating its function as a key reader of the trypanosomatid-tubulin code. Taken together, our work establishes the importance of tubulin detyrosination in remodeling the microtubule-based cytoskeleton required for efficient proliferation in the mammalian host. This highlights tubulin detyrosination as a potential target for therapeutic action against leishmaniasis.
{"title":"Tubulin detyrosination shapes Leishmania cytoskeletal architecture and virulence","authors":"Rosa Milagros Corrales, Jeremy Vincent, Lucien Crobu, Rachel Neish, Binita Nepal, Julien Espeut, Grégoire Pasquier, Ghislain Gillard, Chantal Cazevieille, Jeremy C. Mottram, Dawn M. Wetzel, Yvon Sterkers, Krzysztof Rogowski, Maude F. Lévêque","doi":"10.1073/pnas.2415296122","DOIUrl":"https://doi.org/10.1073/pnas.2415296122","url":null,"abstract":"Tubulin detyrosination has been implicated in various human disorders and is important for regulating microtubule dynamics. While in most organisms this modification is restricted to α-tubulin, in trypanosomatid parasites, it occurs on both α- and β-tubulin. Here, we show that in <jats:italic>Leishmania</jats:italic> , a single vasohibin (LmVASH) enzyme is responsible for differential kinetics of α- and β-tubulin detyrosination. LmVASH knockout parasites, which are completely devoid of detyrosination, show decreased levels of glutamylation and exhibit a strongly diminished pathogenicity in mice, correlating with decreased proliferation in macrophages. Reduced virulence is associated with altered morphogenesis and flagellum remodeling in detyrosination-deficient amastigotes. Flagellum shortening in the absence of detyrosination is caused by hyperactivity of a microtubule-depolymerizing Kinesin-13 homolog, demonstrating its function as a key reader of the trypanosomatid-tubulin code. Taken together, our work establishes the importance of tubulin detyrosination in remodeling the microtubule-based cytoskeleton required for efficient proliferation in the mammalian host. This highlights tubulin detyrosination as a potential target for therapeutic action against leishmaniasis.","PeriodicalId":20548,"journal":{"name":"Proceedings of the National Academy of Sciences of the United States of America","volume":"7 1","pages":""},"PeriodicalIF":11.1,"publicationDate":"2025-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142981588","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-01-14Epub Date: 2024-12-20DOI: 10.1073/pnas.2424914121
{"title":"Correction to Supporting Information for Le et al., Motor neuron disease, TDP-43 pathology, and memory deficits in mice expressing ALS-FTD-linked <i>UBQLN2</i> mutations.","authors":"","doi":"10.1073/pnas.2424914121","DOIUrl":"https://doi.org/10.1073/pnas.2424914121","url":null,"abstract":"","PeriodicalId":20548,"journal":{"name":"Proceedings of the National Academy of Sciences of the United States of America","volume":"122 2","pages":"e2424914121"},"PeriodicalIF":9.4,"publicationDate":"2025-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142869587","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sialic acids derived from colonic mucin glycans are crucial nutrients for enteric bacterial pathogens like Salmonella. The uptake and utilization of sialic acid in Salmonella depend on coordinated regulons, each activated by specific metabolites at the transcriptional level. However, the mechanisms enabling crosstalk among these regulatory circuits to synchronize gene expression remain poorly understood. Here, we identify ManS, a small noncoding RNA derived from the 3' UTR of STM1128 mRNA transcribed from a Salmonella enterica-specific genetic locus, as an important posttranscriptional regulator coordinating sialic acid metabolism regulons. ManS is primarily processed by RNase III and, along with its parental transcripts, is specifically activated by N-acetylmannosamine (ManNAc), the initial degradation product of sialic acid. We found that the imperfect stem-loop structure at the 5' end of ManS allows RNase III to cleave in a noncanonical manner, generating two functional types of ManS with the assistance of RNase E and other RNases: short isoforms with a single seed region that regulate the uptake of N-acetylglucosamine, an essential intermediate in sialic acid metabolism; and long isoforms with an additional seed region that regulate multiple genes involved in central and secondary metabolism. This sophisticated regulation by ManS significantly impacts ManNAc metabolism and S. enterica's competitive behavior during infection. Our findings highlight the role of sRNA in coordinating transcriptional circuits and advance our understanding of RNase III-mediated processing of 3' UTR-derived sRNAs, underscoring the important role of ManNAc in Salmonella adaptation within host environments.
{"title":"An RNase III-processed sRNA coordinates sialic acid metabolism of <i>Salmonella enterica</i> during gut colonization.","authors":"Ziying Chen, Yaomei Yang, Xiaomin Chen, Cheng Bei, Qian Gao, Yanjie Chao, Chuan Wang","doi":"10.1073/pnas.2414563122","DOIUrl":"10.1073/pnas.2414563122","url":null,"abstract":"<p><p>Sialic acids derived from colonic mucin glycans are crucial nutrients for enteric bacterial pathogens like <i>Salmonella</i>. The uptake and utilization of sialic acid in <i>Salmonella</i> depend on coordinated regulons, each activated by specific metabolites at the transcriptional level. However, the mechanisms enabling crosstalk among these regulatory circuits to synchronize gene expression remain poorly understood. Here, we identify ManS, a small noncoding RNA derived from the 3' UTR of <i>STM1128</i> mRNA transcribed from a <i>Salmonella enterica</i>-specific genetic locus, as an important posttranscriptional regulator coordinating sialic acid metabolism regulons. ManS is primarily processed by RNase III and, along with its parental transcripts, is specifically activated by N-acetylmannosamine (ManNAc), the initial degradation product of sialic acid. We found that the imperfect stem-loop structure at the 5' end of ManS allows RNase III to cleave in a noncanonical manner, generating two functional types of ManS with the assistance of RNase E and other RNases: short isoforms with a single seed region that regulate the uptake of N-acetylglucosamine, an essential intermediate in sialic acid metabolism; and long isoforms with an additional seed region that regulate multiple genes involved in central and secondary metabolism. This sophisticated regulation by ManS significantly impacts ManNAc metabolism and <i>S. enterica</i>'s competitive behavior during infection. Our findings highlight the role of sRNA in coordinating transcriptional circuits and advance our understanding of RNase III-mediated processing of 3' UTR-derived sRNAs, underscoring the important role of ManNAc in <i>Salmonella</i> adaptation within host environments.</p>","PeriodicalId":20548,"journal":{"name":"Proceedings of the National Academy of Sciences of the United States of America","volume":"122 2","pages":"e2414563122"},"PeriodicalIF":9.4,"publicationDate":"2025-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142953850","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-01-14Epub Date: 2025-01-10DOI: 10.1073/pnas.2415530121
Ariana Y Tse, Andrew J Spakowitz
DNA methylation is a crucial epigenetic modification that orchestrates chromatin remodelers that suppress transcription, and aberrations in DNA methylation result in a variety of conditions such as cancers and developmental disorders. While it is understood that methylation occurs at CpG-rich DNA regions, it is less understood how distinct methylation profiles are established within various cell types. In this work, we develop a molecular-transport model that depicts the genomic exploration of DNA methyltransferase within a multiscale DNA environment, incorporating biologically relevant factors like methylation rate and CpG density to predict how patterns are established. Our model predicts DNA methylation-state correlation distributions arising from the transport and kinetic properties that are crucial for the establishment of unique methylation profiles. We model the methylation correlation distributions of nine cancerous human cell types to determine how these properties affect the epigenetic profile. Our theory is capable of recapitulating experimental methylation patterns, suggesting the importance of DNA methyltransferase transport in epigenetic regulation. Through this work, we propose a mechanistic description for the establishment of methylation profiles, capturing the key behavioral characteristics of methyltransferase that lead to aberrant methylation.
{"title":"Modeling DNA methyltransferase function to predict epigenetic correlation patterns in healthy and cancer cells.","authors":"Ariana Y Tse, Andrew J Spakowitz","doi":"10.1073/pnas.2415530121","DOIUrl":"10.1073/pnas.2415530121","url":null,"abstract":"<p><p>DNA methylation is a crucial epigenetic modification that orchestrates chromatin remodelers that suppress transcription, and aberrations in DNA methylation result in a variety of conditions such as cancers and developmental disorders. While it is understood that methylation occurs at CpG-rich DNA regions, it is less understood how distinct methylation profiles are established within various cell types. In this work, we develop a molecular-transport model that depicts the genomic exploration of DNA methyltransferase within a multiscale DNA environment, incorporating biologically relevant factors like methylation rate and CpG density to predict how patterns are established. Our model predicts DNA methylation-state correlation distributions arising from the transport and kinetic properties that are crucial for the establishment of unique methylation profiles. We model the methylation correlation distributions of nine cancerous human cell types to determine how these properties affect the epigenetic profile. Our theory is capable of recapitulating experimental methylation patterns, suggesting the importance of DNA methyltransferase transport in epigenetic regulation. Through this work, we propose a mechanistic description for the establishment of methylation profiles, capturing the key behavioral characteristics of methyltransferase that lead to aberrant methylation.</p>","PeriodicalId":20548,"journal":{"name":"Proceedings of the National Academy of Sciences of the United States of America","volume":"122 2","pages":"e2415530121"},"PeriodicalIF":9.4,"publicationDate":"2025-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142953859","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Jifu Duan, Andreas Rutz, Akihiro Kawamoto, Shuvankar Naskar, Kristina Edenharter, Silke Leimkühler, Eckhard Hofmann, Thomas Happe, Genji Kurisu
[FeFe]-hydrogenases catalyze the reversible two-electron reduction of two protons to molecular hydrogen. Although these enzymes are among the most efficient H 2 -converting biocatalysts in nature, their catalytic cofactor (termed H-cluster) is irreversibly destroyed upon contact with dioxygen. The [FeFe]-hydrogenase CbA5H from Clostridium beijerinckii has a unique mechanism to protect the H-cluster from oxygen-induced degradation. The protective strategy of CbA5H was proposed based on a partial protein structure of CbA5H’s oxygen-shielded form. Here, we present a cryo-EM structure of 2.2 Å resolution from the entire enzyme in its dimeric and active state and elucidate the structural parameters of the reversible cofactor protection mechanism. We found that both subunits of the homodimeric structure of CbA5H have a Zn 2+ -binding four-helix domain, which does not play a role in electron transport as described for other complex protein structures. Biochemical data instead confirm that two [4Fe-4S] clusters are responsible for electron transfer in CbA5H, while the identified zinc atom is critical for oligomerization and protein stability.
{"title":"Structural determinants of oxygen resistance and Zn 2+ -mediated stability of the [FeFe]-hydrogenase from Clostridium beijerinckii","authors":"Jifu Duan, Andreas Rutz, Akihiro Kawamoto, Shuvankar Naskar, Kristina Edenharter, Silke Leimkühler, Eckhard Hofmann, Thomas Happe, Genji Kurisu","doi":"10.1073/pnas.2416233122","DOIUrl":"https://doi.org/10.1073/pnas.2416233122","url":null,"abstract":"[FeFe]-hydrogenases catalyze the reversible two-electron reduction of two protons to molecular hydrogen. Although these enzymes are among the most efficient H <jats:sub>2</jats:sub> -converting biocatalysts in nature, their catalytic cofactor (termed H-cluster) is irreversibly destroyed upon contact with dioxygen. The [FeFe]-hydrogenase CbA5H from <jats:italic>Clostridium beijerinckii</jats:italic> has a unique mechanism to protect the H-cluster from oxygen-induced degradation. The protective strategy of CbA5H was proposed based on a partial protein structure of CbA5H’s oxygen-shielded form. Here, we present a cryo-EM structure of 2.2 Å resolution from the entire enzyme in its dimeric and active state and elucidate the structural parameters of the reversible cofactor protection mechanism. We found that both subunits of the homodimeric structure of CbA5H have a Zn <jats:sup>2+</jats:sup> -binding four-helix domain, which does not play a role in electron transport as described for other complex protein structures. Biochemical data instead confirm that two [4Fe-4S] clusters are responsible for electron transfer in CbA5H, while the identified zinc atom is critical for oligomerization and protein stability.","PeriodicalId":20548,"journal":{"name":"Proceedings of the National Academy of Sciences of the United States of America","volume":"45 14 1","pages":""},"PeriodicalIF":11.1,"publicationDate":"2025-01-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142974855","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Bradley G. Lusk, Sheba Morgan, Shawn P. Mulvaney, Brandon Blue, Sam W. LaGasse, Cory D. Cress, Jesper T. Bjerg, Woo K. Lee, Brian J. Eddie, Jeremy T. Robinson
This study presents the direct measurement of proton transport along filamentous Desulfobulbaceae , or cable bacteria. Cable bacteria are filamentous multicellular microorganisms that have garnered much interest due to their ability to serve as electrical conduits, transferring electrons over several millimeters. Our results indicate that cable bacteria can also function as protonic conduits because they contain proton wires that transport protons at distances >100 µm. We find that protonic conductivity (σ P ) along cable bacteria varies between samples and is measured as high as 114 ± 28 µS cm −1 at 25 °C and 70% relative humidity (RH). For cable bacteria, the protonic conductance (G P ) and σ P are dependent upon the RH, increasing by as much as 26-fold between 60% and 80% RH. This observation implies that proton transport occurs via the Grotthuss mechanism along water associated with cable bacteria, forming proton wires. In order to determine σ P and G P along cable bacteria, we implemented a protocol using a modified transfer-printing technique to deposit either palladium interdigitated protodes (IDP), palladium transfer length method (TLM) protodes, or gold interdigitated electrodes (IDE) on top of cable bacteria. Due to the relatively mild nature of the transfer-printing technique, this method should be applicable to a broad array of biological samples and curved materials. The observation of protonic conductivity in cable bacteria presents possibilities for investigating the importance of long-distance proton transport in microbial ecosystems and to potentially build biotic or biomimetic scaffolds to interface with materials via proton-mediated gateways or channels.
{"title":"Hydrated cable bacteria exhibit protonic conductivity over long distances","authors":"Bradley G. Lusk, Sheba Morgan, Shawn P. Mulvaney, Brandon Blue, Sam W. LaGasse, Cory D. Cress, Jesper T. Bjerg, Woo K. Lee, Brian J. Eddie, Jeremy T. Robinson","doi":"10.1073/pnas.2416008122","DOIUrl":"https://doi.org/10.1073/pnas.2416008122","url":null,"abstract":"This study presents the direct measurement of proton transport along filamentous <jats:italic>Desulfobulbaceae</jats:italic> , or cable bacteria. Cable bacteria are filamentous multicellular microorganisms that have garnered much interest due to their ability to serve as electrical conduits, transferring electrons over several millimeters. Our results indicate that cable bacteria can also function as protonic conduits because they contain proton wires that transport protons at distances >100 µm. We find that protonic conductivity (σ <jats:italic> <jats:sub>P</jats:sub> </jats:italic> ) along cable bacteria varies between samples and is measured as high as 114 ± 28 µS cm <jats:sup>−1</jats:sup> at 25 °C and 70% relative humidity (RH). For cable bacteria, the protonic conductance (G <jats:italic> <jats:sub>P</jats:sub> </jats:italic> ) and σ <jats:italic> <jats:sub>P</jats:sub> </jats:italic> are dependent upon the RH, increasing by as much as 26-fold between 60% and 80% RH. This observation implies that proton transport occurs via the Grotthuss mechanism along water associated with cable bacteria, forming proton wires. In order to determine σ <jats:italic> <jats:sub>P</jats:sub> </jats:italic> and G <jats:italic> <jats:sub>P</jats:sub> </jats:italic> along cable bacteria, we implemented a protocol using a modified transfer-printing technique to deposit either palladium interdigitated protodes (IDP), palladium transfer length method (TLM) protodes, or gold interdigitated electrodes (IDE) on top of cable bacteria. Due to the relatively mild nature of the transfer-printing technique, this method should be applicable to a broad array of biological samples and curved materials. The observation of protonic conductivity in cable bacteria presents possibilities for investigating the importance of long-distance proton transport in microbial ecosystems and to potentially build biotic or biomimetic scaffolds to interface with materials via proton-mediated gateways or channels.","PeriodicalId":20548,"journal":{"name":"Proceedings of the National Academy of Sciences of the United States of America","volume":"29 1","pages":""},"PeriodicalIF":11.1,"publicationDate":"2025-01-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142974853","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sandra Bibiana Correa, Karold V. Coronado-Franco, Celine Jézéquel, Amanda Cantarute Rodrigues, Kristine O. Evans, Joshua J. Granger, Hans Ter Steege, Iêda Leão do Amaral, Luiz de Souza Coelho, Florian Wittmann, Francisca Dionízia de Almeida Matos, Diógenes de Andrade Lima Filho, Rafael P. Salomão, Carolina V. Castilho, Juan Ernesto Guevara, Marcelo de Jesus Veiga Carim, Oliver L. Phillips, Maria Teresa Fernandez Piedade, Layon O. Demarchi, Jochen Schöngart, Juan David Cardenas Revilla, Maria Pires Martins, Mariana Victória Irume, José Renan da Silva Guimarães, José Ferreira Ramos, Adriano Costa Quaresma, Nigel C. A. Pitman, Bruno Garcia Luize, Evlyn Márcia Moraes de Leão Novo, Eduardo Martins Venticinque, Thiago Sanna Freire Silva, Percy Núñez Vargas, Angelo Gilberto Manzatto, Neidiane Farias Costa Reis, John Terborgh, Katia Regina Casula, Euridice N. Honorio Coronado, Juan Carlos Montero, Abel Monteagudo Mendoza, Ted R. Feldpausch, Flávia Machado Durgante, Nicolás Castaño Arboleda, Beatriz S. Marimon, Ben Hur Marimon-Junior, Timothy J. Killeen, Rodolfo Vasquez, Bonifacio Mostacedo, Rafael L. Assis, Dário Dantas do Amaral, John Ethan Householder, Marcelo Fragomeni Simon, Marcelo Brilhante de Medeiros, Helder Lima de Queiroz, Maria Aparecida Lopes, José Leonardo Lima Magalhães, Pablo R. Stevenson, Bruno Barçante Ladvocat Cintra, Alejandro Araujo-Murakami, Tim R. Baker, Yuri Oliveira Feitosa, Hugo F. Mogollón, Joost F. Duivenvoorden, Leandro Valle Ferreira, José Julio de Toledo, James A. Comiskey, Aline Lopes, Gabriel Damasco, Alberto Vicentini, Fernando Cornejo Valverde, Vitor H. F. Gomes, Alfonso Alonso, Francisco Dallmeier, Daniel P. P. de Aguiar, Rogerio Gribel, Juan Carlos Licona, Boris Eduardo Villa Zegarra, Marcelino Carneiro Guedes, Carlos Cerón, Raquel Thomas, William Milliken, Wegliane Campelo, Bianca Weiss Albuquerque, Bente Klitgaard, J. Sebastián Tello, Alfredo Fuentes Claros, Gonzalo Rivas-Torres, Juan Fernando Phillips, Patricio von Hildebrand, Therany Gonzales, César I. A. Vela, Bruce Hoffman, Bernardo Monteiro Flores, Maihyra Marina Pombo, Maira Rocha, Milena Holmgren, Angela Cano, Maria Natalia Umaña, Luisa Fernanda Casas, Henrik Balslev, Ligia Estela Urrego Giraldo, Rémy Bigorne, Thierry Oberdorff, Javier A. Maldonado-Ocampo, Hernan Ortega, Max Hidalgo, Koen Martens, Gislene Torrente-Vilara, Jansen Zuanon, Astrid Acosta, Edwin Agudelo, Soraya Barrera Maure, Douglas A. Bastos, Juan Bogotá Gregory, Fernando G. Cabeceira, André L. C. Canto, Fernando M. Carvajal-Vallejos, Lucélia N. Carvalho, Ariana Cella-Ribeiro, Raphaël Covain, Murilo S. Dias, Carlos Donascimiento, Carolina R. C. Dória, Cleber Duarte, Efrem J. G. Ferreira, André V. Galuch, Tommaso Giarrizzo, Rafael P. Leitão, John G. Lundberg, Mabel Maldonado, José I. Mojica, Luciano F. A. Montag, William Ohara, Tiago H. S. Pires, Marc Pouilly, Saúl Prada-Pedreros, Luiz J. de Queiroz, Lucia Rapp Py-Daniel, Frank R. V. Ribeiro, Raúl Ríos Herrera, Marcelo Rodrigues dos Anjos, Igor Hister Lourenco, Jaime Sarmiento, Leandro M. Sousa, Lis F. Stegmann, Jonathan Valdiviezo-Rivera, Francisco Villa, Takayuki Yunoki, Pablo A. Tedesco
Unlike most rivers globally, nearly all lowland Amazonian rivers have unregulated flow, supporting seasonally flooded floodplain forests. Floodplain forests harbor a unique tree species assemblage adapted to flooding and specialized fauna, including fruit-eating fish that migrate seasonally into floodplains, favoring expansive floodplain areas. Frugivorous fish are forest-dependent fauna critical to forest regeneration via seed dispersal and support commercial and artisanal fisheries. We implemented linear mixed effects models to investigate drivers of species richness among specialized frugivorous fishes across the ~6,000,000 km 2 Amazon Basin, analyzing 29 species from 9 families (10,058 occurrences). Floodplain predictors per subbasin included floodplain forest extent, tree species richness (309,540 occurrences for 2,506 species), water biogeochemistry, flood duration, and elevation, with river order controlling for longitudinal positioning along the river network. We observed heterogeneous patterns of frugivorous fish species richness, which were positively correlated with floodplain forest extent, tree species richness, and flood duration. The natural hydrological regime facilitates fish access to flooded forests and controls fruit production. Thus, the ability of Amazonian floodplain ecosystems to support frugivorous fish assemblages hinges on extensive and diverse seasonally flooded forests. Given the low functional redundancy in fish seed dispersal networks, diverse frugivorous fish assemblages disperse and maintain diverse forests; vice versa, diverse forests maintain more fish species, underscoring the critically important taxonomic interdependencies that embody Amazonian ecosystems. Effective management strategies must acknowledge that access to diverse and hydrologically functional floodplain forests is essential to ensure the long-term survival of frugivorous fish and, in turn, the long-term sustainability of floodplain forests.
{"title":"Floodplain forests drive fruit-eating fish diversity at the Amazon Basin-scale","authors":"Sandra Bibiana Correa, Karold V. Coronado-Franco, Celine Jézéquel, Amanda Cantarute Rodrigues, Kristine O. Evans, Joshua J. Granger, Hans Ter Steege, Iêda Leão do Amaral, Luiz de Souza Coelho, Florian Wittmann, Francisca Dionízia de Almeida Matos, Diógenes de Andrade Lima Filho, Rafael P. Salomão, Carolina V. Castilho, Juan Ernesto Guevara, Marcelo de Jesus Veiga Carim, Oliver L. Phillips, Maria Teresa Fernandez Piedade, Layon O. Demarchi, Jochen Schöngart, Juan David Cardenas Revilla, Maria Pires Martins, Mariana Victória Irume, José Renan da Silva Guimarães, José Ferreira Ramos, Adriano Costa Quaresma, Nigel C. A. Pitman, Bruno Garcia Luize, Evlyn Márcia Moraes de Leão Novo, Eduardo Martins Venticinque, Thiago Sanna Freire Silva, Percy Núñez Vargas, Angelo Gilberto Manzatto, Neidiane Farias Costa Reis, John Terborgh, Katia Regina Casula, Euridice N. Honorio Coronado, Juan Carlos Montero, Abel Monteagudo Mendoza, Ted R. Feldpausch, Flávia Machado Durgante, Nicolás Castaño Arboleda, Beatriz S. Marimon, Ben Hur Marimon-Junior, Timothy J. Killeen, Rodolfo Vasquez, Bonifacio Mostacedo, Rafael L. Assis, Dário Dantas do Amaral, John Ethan Householder, Marcelo Fragomeni Simon, Marcelo Brilhante de Medeiros, Helder Lima de Queiroz, Maria Aparecida Lopes, José Leonardo Lima Magalhães, Pablo R. Stevenson, Bruno Barçante Ladvocat Cintra, Alejandro Araujo-Murakami, Tim R. Baker, Yuri Oliveira Feitosa, Hugo F. Mogollón, Joost F. Duivenvoorden, Leandro Valle Ferreira, José Julio de Toledo, James A. Comiskey, Aline Lopes, Gabriel Damasco, Alberto Vicentini, Fernando Cornejo Valverde, Vitor H. F. Gomes, Alfonso Alonso, Francisco Dallmeier, Daniel P. P. de Aguiar, Rogerio Gribel, Juan Carlos Licona, Boris Eduardo Villa Zegarra, Marcelino Carneiro Guedes, Carlos Cerón, Raquel Thomas, William Milliken, Wegliane Campelo, Bianca Weiss Albuquerque, Bente Klitgaard, J. Sebastián Tello, Alfredo Fuentes Claros, Gonzalo Rivas-Torres, Juan Fernando Phillips, Patricio von Hildebrand, Therany Gonzales, César I. A. Vela, Bruce Hoffman, Bernardo Monteiro Flores, Maihyra Marina Pombo, Maira Rocha, Milena Holmgren, Angela Cano, Maria Natalia Umaña, Luisa Fernanda Casas, Henrik Balslev, Ligia Estela Urrego Giraldo, Rémy Bigorne, Thierry Oberdorff, Javier A. Maldonado-Ocampo, Hernan Ortega, Max Hidalgo, Koen Martens, Gislene Torrente-Vilara, Jansen Zuanon, Astrid Acosta, Edwin Agudelo, Soraya Barrera Maure, Douglas A. Bastos, Juan Bogotá Gregory, Fernando G. Cabeceira, André L. C. Canto, Fernando M. Carvajal-Vallejos, Lucélia N. Carvalho, Ariana Cella-Ribeiro, Raphaël Covain, Murilo S. Dias, Carlos Donascimiento, Carolina R. C. Dória, Cleber Duarte, Efrem J. G. Ferreira, André V. Galuch, Tommaso Giarrizzo, Rafael P. Leitão, John G. Lundberg, Mabel Maldonado, José I. Mojica, Luciano F. A. Montag, William Ohara, Tiago H. S. Pires, Marc Pouilly, Saúl Prada-Pedreros, Luiz J. de Queiroz, Lucia Rapp Py-Daniel, Frank R. V. Ribeiro, Raúl Ríos Herrera, Marcelo Rodrigues dos Anjos, Igor Hister Lourenco, Jaime Sarmiento, Leandro M. Sousa, Lis F. Stegmann, Jonathan Valdiviezo-Rivera, Francisco Villa, Takayuki Yunoki, Pablo A. Tedesco","doi":"10.1073/pnas.2414416122","DOIUrl":"https://doi.org/10.1073/pnas.2414416122","url":null,"abstract":"Unlike most rivers globally, nearly all lowland Amazonian rivers have unregulated flow, supporting seasonally flooded floodplain forests. Floodplain forests harbor a unique tree species assemblage adapted to flooding and specialized fauna, including fruit-eating fish that migrate seasonally into floodplains, favoring expansive floodplain areas. Frugivorous fish are forest-dependent fauna critical to forest regeneration via seed dispersal and support commercial and artisanal fisheries. We implemented linear mixed effects models to investigate drivers of species richness among specialized frugivorous fishes across the ~6,000,000 km <jats:sup>2</jats:sup> Amazon Basin, analyzing 29 species from 9 families (10,058 occurrences). Floodplain predictors per subbasin included floodplain forest extent, tree species richness (309,540 occurrences for 2,506 species), water biogeochemistry, flood duration, and elevation, with river order controlling for longitudinal positioning along the river network. We observed heterogeneous patterns of frugivorous fish species richness, which were positively correlated with floodplain forest extent, tree species richness, and flood duration. The natural hydrological regime facilitates fish access to flooded forests and controls fruit production. Thus, the ability of Amazonian floodplain ecosystems to support frugivorous fish assemblages hinges on extensive and diverse seasonally flooded forests. Given the low functional redundancy in fish seed dispersal networks, diverse frugivorous fish assemblages disperse and maintain diverse forests; vice versa, diverse forests maintain more fish species, underscoring the critically important taxonomic interdependencies that embody Amazonian ecosystems. Effective management strategies must acknowledge that access to diverse and hydrologically functional floodplain forests is essential to ensure the long-term survival of frugivorous fish and, in turn, the long-term sustainability of floodplain forests.","PeriodicalId":20548,"journal":{"name":"Proceedings of the National Academy of Sciences of the United States of America","volume":"45 1","pages":""},"PeriodicalIF":11.1,"publicationDate":"2025-01-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142974859","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Thomas G. Kaye, Judyta Bąk, Henry William Marcelo, Michael Pittman
Tattoos were a prevalent art form in pre-Hispanic South America exemplified by mummified human remains with preserved skin decoration that reflects the personal and cultural representations of their times. Tattoos are known to fade and bleed over time and this is compounded in mummies by the decay of the body, inhibiting the ability to examine the original art. Laser-stimulated fluorescence (LSF) produces images based on fluorescence emitted from within the target. Here, we present the first results of applying LSF to tattoos on human remains from the pre-Columbian Chancay culture of coastal Peru. We find that the preserved skin fluoresced strongly underneath the black tattoo ink yielding a high-contrast image that virtually eliminates the ink bleed, revealing the exceptionally fine details of the original artwork. The level of detail and precision of the artwork was found to be higher than associated pottery, textiles, and rock art suggesting special effort was expended by the Chancay on at least some of their tattoos. This suggests artistic complexity in pre-Columbian Peru was at a higher level than previously known, expanding the degree of artistic development found in South America at this time. LSF expands the scope of tattoo analysis and the level of detail this can yield providing a new technique to gain further insights into this important art form.
{"title":"Hidden artistic complexity of Peru’s Chancay culture discovered in tattoos by laser-stimulated fluorescence","authors":"Thomas G. Kaye, Judyta Bąk, Henry William Marcelo, Michael Pittman","doi":"10.1073/pnas.2421517122","DOIUrl":"https://doi.org/10.1073/pnas.2421517122","url":null,"abstract":"Tattoos were a prevalent art form in pre-Hispanic South America exemplified by mummified human remains with preserved skin decoration that reflects the personal and cultural representations of their times. Tattoos are known to fade and bleed over time and this is compounded in mummies by the decay of the body, inhibiting the ability to examine the original art. Laser-stimulated fluorescence (LSF) produces images based on fluorescence emitted from within the target. Here, we present the first results of applying LSF to tattoos on human remains from the pre-Columbian Chancay culture of coastal Peru. We find that the preserved skin fluoresced strongly underneath the black tattoo ink yielding a high-contrast image that virtually eliminates the ink bleed, revealing the exceptionally fine details of the original artwork. The level of detail and precision of the artwork was found to be higher than associated pottery, textiles, and rock art suggesting special effort was expended by the Chancay on at least some of their tattoos. This suggests artistic complexity in pre-Columbian Peru was at a higher level than previously known, expanding the degree of artistic development found in South America at this time. LSF expands the scope of tattoo analysis and the level of detail this can yield providing a new technique to gain further insights into this important art form.","PeriodicalId":20548,"journal":{"name":"Proceedings of the National Academy of Sciences of the United States of America","volume":"29 1","pages":""},"PeriodicalIF":11.1,"publicationDate":"2025-01-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142975150","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
James A. Howard, Lucija Hok, Richard L. Cate, Nathaniel J. Sanford, Kaitlin N. Hart, Edmund A. E. Leach, Alena S. Bruening, Nicholas Nagykery, Patricia K. Donahoe, David Pépin, Thomas B. Thompson
TGFβ family ligands are synthesized as precursors consisting of an N-terminal prodomain and C-terminal growth factor (GF) signaling domain. After proteolytic processing, the prodomain typically remains noncovalently associated with the GF, sometimes forming a high-affinity latent procomplex that requires activation. For the TGFβ family ligand anti-Müllerian hormone (AMH), the prodomain maintains a high-affinity interaction with its GF that does not render it latent. While the prodomain can be displaced by the type II receptor, AMHR2, the nature of the GF:prodomain interaction and the mechanism of prodomain displacement by AMHR2 are currently unknown. We show here that the AMH prodomain exhibits an atypical two-domain structure, containing a dimerizing and a GF-binding domain connected through a flexible linker. Cryo-EM and genomic analyses show that the distinctive GF-binding domain, the result of an exon insertion 450 Mya, comprises a helical bundle and a belt-like structure which interact with the GF at the type II and I receptor binding sites, respectively. The dimerizing domain, which adopts a TGFβ-like propeptide fold, covalently connects two prodomains through intermolecular disulfide bonds. Disease mutations map to both the GF-binding and dimerization domains. Our results support a model where AMHR2 displaces the helical bundle and induces a conformational change in the GF, followed by release of the prodomain and engagement of the type I receptor. Collectively, this study shows that the AMH prodomain has evolved an atypical binding interaction with the GF that favors, without disrupting signaling, the maintenance of a noncovalent complex until receptors are engaged.
{"title":"A divergent two-domain structure of the anti-Müllerian hormone prodomain","authors":"James A. Howard, Lucija Hok, Richard L. Cate, Nathaniel J. Sanford, Kaitlin N. Hart, Edmund A. E. Leach, Alena S. Bruening, Nicholas Nagykery, Patricia K. Donahoe, David Pépin, Thomas B. Thompson","doi":"10.1073/pnas.2418088122","DOIUrl":"https://doi.org/10.1073/pnas.2418088122","url":null,"abstract":"TGFβ family ligands are synthesized as precursors consisting of an N-terminal prodomain and C-terminal growth factor (GF) signaling domain. After proteolytic processing, the prodomain typically remains noncovalently associated with the GF, sometimes forming a high-affinity latent procomplex that requires activation. For the TGFβ family ligand anti-Müllerian hormone (AMH), the prodomain maintains a high-affinity interaction with its GF that does not render it latent. While the prodomain can be displaced by the type II receptor, AMHR2, the nature of the GF:prodomain interaction and the mechanism of prodomain displacement by AMHR2 are currently unknown. We show here that the AMH prodomain exhibits an atypical two-domain structure, containing a dimerizing and a GF-binding domain connected through a flexible linker. Cryo-EM and genomic analyses show that the distinctive GF-binding domain, the result of an exon insertion 450 Mya, comprises a helical bundle and a belt-like structure which interact with the GF at the type II and I receptor binding sites, respectively. The dimerizing domain, which adopts a TGFβ-like propeptide fold, covalently connects two prodomains through intermolecular disulfide bonds. Disease mutations map to both the GF-binding and dimerization domains. Our results support a model where AMHR2 displaces the helical bundle and induces a conformational change in the GF, followed by release of the prodomain and engagement of the type I receptor. Collectively, this study shows that the AMH prodomain has evolved an atypical binding interaction with the GF that favors, without disrupting signaling, the maintenance of a noncovalent complex until receptors are engaged.","PeriodicalId":20548,"journal":{"name":"Proceedings of the National Academy of Sciences of the United States of America","volume":"19 1","pages":""},"PeriodicalIF":11.1,"publicationDate":"2025-01-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142975151","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Peter F. Chuckran, Katerina Estera-Molina, Alexa M. Nicolas, Ella T. Sieradzki, Paul Dijkstra, Mary K. Firestone, Jennifer Pett-Ridge, Steven J. Blazewicz
In soils, the first rain after a prolonged dry period represents a major pulse event impacting soil microbial community function, yet we lack a full understanding of the genomic traits associated with the microbial response to rewetting. Genomic traits such as codon usage bias and genome size have been linked to bacterial growth in soils—however, often through measurements in culture. Here, we used metagenome-assembled genomes (MAGs) with 18 O-water stable isotope probing and metatranscriptomics to track genomic traits associated with growth and transcription of soil microorganisms over one week following rewetting of a grassland soil. We found that codon bias in ribosomal protein genes was the strongest predictor of growth rate. We also found higher growth rates in bacteria with smaller genomes, suggesting that reduced genome size enables a faster response to pulses in soil bacteria. Faster transcriptional upregulation of ribosomal protein genes was associated with high codon bias and increased nucleotide skew. We found that several of these relationships existed within phyla, indicating that these associations between genomic traits and activity could be generalized characteristics of soil bacteria. Finally, we used publicly available metagenomes to assess the distribution of codon bias across a pH gradient and found that microbial communities in higher pH soils—which are often more water limited and pulse driven—have higher codon usage bias in their ribosomal protein genes. Together, these results provide evidence that genomic characteristics affect soil microbial activity during rewetting and pose a potential fitness advantage for soil bacteria where water and nutrient availability are episodic.
{"title":"Codon bias, nucleotide selection, and genome size predict in situ bacterial growth rate and transcription in rewetted soil","authors":"Peter F. Chuckran, Katerina Estera-Molina, Alexa M. Nicolas, Ella T. Sieradzki, Paul Dijkstra, Mary K. Firestone, Jennifer Pett-Ridge, Steven J. Blazewicz","doi":"10.1073/pnas.2413032122","DOIUrl":"https://doi.org/10.1073/pnas.2413032122","url":null,"abstract":"In soils, the first rain after a prolonged dry period represents a major pulse event impacting soil microbial community function, yet we lack a full understanding of the genomic traits associated with the microbial response to rewetting. Genomic traits such as codon usage bias and genome size have been linked to bacterial growth in soils—however, often through measurements in culture. Here, we used metagenome-assembled genomes (MAGs) with <jats:sup>18</jats:sup> O-water stable isotope probing and metatranscriptomics to track genomic traits associated with growth and transcription of soil microorganisms over one week following rewetting of a grassland soil. We found that codon bias in ribosomal protein genes was the strongest predictor of growth rate. We also found higher growth rates in bacteria with smaller genomes, suggesting that reduced genome size enables a faster response to pulses in soil bacteria. Faster transcriptional upregulation of ribosomal protein genes was associated with high codon bias and increased nucleotide skew. We found that several of these relationships existed within phyla, indicating that these associations between genomic traits and activity could be generalized characteristics of soil bacteria. Finally, we used publicly available metagenomes to assess the distribution of codon bias across a pH gradient and found that microbial communities in higher pH soils—which are often more water limited and pulse driven—have higher codon usage bias in their ribosomal protein genes. Together, these results provide evidence that genomic characteristics affect soil microbial activity during rewetting and pose a potential fitness advantage for soil bacteria where water and nutrient availability are episodic.","PeriodicalId":20548,"journal":{"name":"Proceedings of the National Academy of Sciences of the United States of America","volume":"22 1","pages":""},"PeriodicalIF":11.1,"publicationDate":"2025-01-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142975155","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
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