The UlaG protein familly defines novel structural and functional motifs grafted on an ancient RNase fold

Background: Bacterial populations are highly successful at colonizing new habitats and adapting to changing environmental conditions, partly due to their capacity to evolve novel virulence and metabolic pathways in response to stress conditions and to shuffle them by horizontal gene transfer (HGT)....

Descripción completa

Detalles Bibliográficos
Autores: Fernández Pérez, Francisco José, Garces, Fernando, López-Estepa, Miguel, Aguilar Piera, Juan, Baldomà Llavinés, Laura, Coll, Miquel, Badía Palacín, Josefa, Vega Fernández, Maria Cristina
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2011
País:España
Institución:Universidad de Barcelona
Repositorio:Dipòsit Digital de la UB
OAI Identifier:oai:diposit.ub.edu:2445/33552
Acceso en línea:https://hdl.handle.net/2445/33552
Access Level:acceso abierto
Palabra clave:Bacteris
Enzims
Filogènia
Bacteria
Enzymes
Phylogeny
Evolució molecular
Molecular evolution
Ribonucleases
Genètica bacteriana
Bacterial genetics
Seqüència d'aminoàcids
Amino acid sequence
id ES_7408cf8950e7d2b2f6fe1f18b8a96dd2
oai_identifier_str oai:diposit.ub.edu:2445/33552
network_acronym_str ES
network_name_str España
repository_id_str
spelling The UlaG protein familly defines novel structural and functional motifs grafted on an ancient RNase foldFernández Pérez, Francisco JoséGarces, FernandoLópez-Estepa, MiguelAguilar Piera, JuanBaldomà Llavinés, LauraColl, MiquelBadía Palacín, JosefaVega Fernández, Maria CristinaBacterisEnzimsFilogèniaBacteriaEnzymesPhylogenyEvolució molecularMolecular evolutionRibonucleasesGenètica bacterianaBacterial geneticsSeqüència d'aminoàcidsAmino acid sequenceBackground: Bacterial populations are highly successful at colonizing new habitats and adapting to changing environmental conditions, partly due to their capacity to evolve novel virulence and metabolic pathways in response to stress conditions and to shuffle them by horizontal gene transfer (HGT). A common theme in the evolution of new functions consists of gene duplication followed by functional divergence. UlaG, a unique manganese-dependent metallo-b-lactamase (MBL) enzyme involved in L-ascorbate metabolism by commensal and symbiotic enterobacteria, provides a model for the study of the emergence of new catalytic activities from the modification of an ancient fold. Furthermore, UlaG is the founding member of the so-called UlaG-like (UlaGL) protein family, a recently established and poorly characterized family comprising divalent (and perhaps trivalent)metal-binding MBLs that catalyze transformations on phosphorylated sugars and nucleotides. Results: Here we combined protein structure-guided and sequence-only molecular phylogenetic analyses to dissect the molecular evolution of UlaG and to study its phylogenomic distribution, its relatedness with present-day UlaGL protein sequences and functional conservation. Phylogenetic analyses indicate that UlaGL sequences are present in Bacteria and Archaea, with bona fide orthologs found mainly in mammalian and plant-associated Gramnegative and Gram-positive bacteria. The incongruence between the UlaGL tree and known species trees indicates exchange by HGT and suggests that the UlaGL-encoding genes provided a growth advantage under changing conditions. Our search for more distantly related protein sequences aided by structural homology has uncovered that UlaGL sequences have a common evolutionary origin with present-day RNA processing and metabolizing MBL enzymes widespread in Bacteria, Archaea, and Eukarya. This observation suggests an ancient origin for the UlaGL family within the broader trunk of the MBL superfamily by duplication, neofunctionalization and fixation. Conclusions: Our results suggest that the forerunner of UlaG was present as an RNA metabolizing enzyme in the last common ancestor, and that the modern descendants of that ancestral gene have a wide phylogenetic distribution and functional roles. We propose that the UlaGL family evolved new metabolic roles among bacterial and possibly archeal phyla in the setting of a close association with metazoans, such as in the mammalian gastrointestinal tract or in animal and plant pathogens, as well as in environmental settings. Accordingly, the major evolutionary forces shaping the UlaGL family include vertical inheritance and lineage-specific duplication and acquisition of novel metabolic functions, followed by HGT and numerous lineage-specific gene loss events.BioMed Central2011info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfhttps://hdl.handle.net/2445/33552Articles publicats en revistes (Bioquímica i Biomedicina Molecular)reponame:Dipòsit Digital de la UBinstname:Universidad de BarcelonaInglésReproducció del document publicat a: http://dx.doi.org/10.1186/1471-2148-11-273Bmc Evolutionary Biology, 2011, vol. 11, num. 273http://dx.doi.org/10.1186/1471-2148-11-273cc-by (c) Fernández Pérez, Francisco José et al., 2011http://creativecommons.org/licenses/by/3.0/esinfo:eu-repo/semantics/openAccessoai:diposit.ub.edu:2445/335522026-05-27T06:46:51Z
dc.title.none.fl_str_mv The UlaG protein familly defines novel structural and functional motifs grafted on an ancient RNase fold
title The UlaG protein familly defines novel structural and functional motifs grafted on an ancient RNase fold
spellingShingle The UlaG protein familly defines novel structural and functional motifs grafted on an ancient RNase fold
Fernández Pérez, Francisco José
Bacteris
Enzims
Filogènia
Bacteria
Enzymes
Phylogeny
Evolució molecular
Molecular evolution
Ribonucleases
Genètica bacteriana
Bacterial genetics
Seqüència d'aminoàcids
Amino acid sequence
title_short The UlaG protein familly defines novel structural and functional motifs grafted on an ancient RNase fold
title_full The UlaG protein familly defines novel structural and functional motifs grafted on an ancient RNase fold
title_fullStr The UlaG protein familly defines novel structural and functional motifs grafted on an ancient RNase fold
title_full_unstemmed The UlaG protein familly defines novel structural and functional motifs grafted on an ancient RNase fold
title_sort The UlaG protein familly defines novel structural and functional motifs grafted on an ancient RNase fold
dc.creator.none.fl_str_mv Fernández Pérez, Francisco José
Garces, Fernando
López-Estepa, Miguel
Aguilar Piera, Juan
Baldomà Llavinés, Laura
Coll, Miquel
Badía Palacín, Josefa
Vega Fernández, Maria Cristina
author Fernández Pérez, Francisco José
author_facet Fernández Pérez, Francisco José
Garces, Fernando
López-Estepa, Miguel
Aguilar Piera, Juan
Baldomà Llavinés, Laura
Coll, Miquel
Badía Palacín, Josefa
Vega Fernández, Maria Cristina
author_role author
author2 Garces, Fernando
López-Estepa, Miguel
Aguilar Piera, Juan
Baldomà Llavinés, Laura
Coll, Miquel
Badía Palacín, Josefa
Vega Fernández, Maria Cristina
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Bacteris
Enzims
Filogènia
Bacteria
Enzymes
Phylogeny
Evolució molecular
Molecular evolution
Ribonucleases
Genètica bacteriana
Bacterial genetics
Seqüència d'aminoàcids
Amino acid sequence
topic Bacteris
Enzims
Filogènia
Bacteria
Enzymes
Phylogeny
Evolució molecular
Molecular evolution
Ribonucleases
Genètica bacteriana
Bacterial genetics
Seqüència d'aminoàcids
Amino acid sequence
description Background: Bacterial populations are highly successful at colonizing new habitats and adapting to changing environmental conditions, partly due to their capacity to evolve novel virulence and metabolic pathways in response to stress conditions and to shuffle them by horizontal gene transfer (HGT). A common theme in the evolution of new functions consists of gene duplication followed by functional divergence. UlaG, a unique manganese-dependent metallo-b-lactamase (MBL) enzyme involved in L-ascorbate metabolism by commensal and symbiotic enterobacteria, provides a model for the study of the emergence of new catalytic activities from the modification of an ancient fold. Furthermore, UlaG is the founding member of the so-called UlaG-like (UlaGL) protein family, a recently established and poorly characterized family comprising divalent (and perhaps trivalent)metal-binding MBLs that catalyze transformations on phosphorylated sugars and nucleotides. Results: Here we combined protein structure-guided and sequence-only molecular phylogenetic analyses to dissect the molecular evolution of UlaG and to study its phylogenomic distribution, its relatedness with present-day UlaGL protein sequences and functional conservation. Phylogenetic analyses indicate that UlaGL sequences are present in Bacteria and Archaea, with bona fide orthologs found mainly in mammalian and plant-associated Gramnegative and Gram-positive bacteria. The incongruence between the UlaGL tree and known species trees indicates exchange by HGT and suggests that the UlaGL-encoding genes provided a growth advantage under changing conditions. Our search for more distantly related protein sequences aided by structural homology has uncovered that UlaGL sequences have a common evolutionary origin with present-day RNA processing and metabolizing MBL enzymes widespread in Bacteria, Archaea, and Eukarya. This observation suggests an ancient origin for the UlaGL family within the broader trunk of the MBL superfamily by duplication, neofunctionalization and fixation. Conclusions: Our results suggest that the forerunner of UlaG was present as an RNA metabolizing enzyme in the last common ancestor, and that the modern descendants of that ancestral gene have a wide phylogenetic distribution and functional roles. We propose that the UlaGL family evolved new metabolic roles among bacterial and possibly archeal phyla in the setting of a close association with metazoans, such as in the mammalian gastrointestinal tract or in animal and plant pathogens, as well as in environmental settings. Accordingly, the major evolutionary forces shaping the UlaGL family include vertical inheritance and lineage-specific duplication and acquisition of novel metabolic functions, followed by HGT and numerous lineage-specific gene loss events.
publishDate 2011
dc.date.none.fl_str_mv 2011
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://hdl.handle.net/2445/33552
url https://hdl.handle.net/2445/33552
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Reproducció del document publicat a: http://dx.doi.org/10.1186/1471-2148-11-273
Bmc Evolutionary Biology, 2011, vol. 11, num. 273
http://dx.doi.org/10.1186/1471-2148-11-273
dc.rights.none.fl_str_mv cc-by (c) Fernández Pérez, Francisco José et al., 2011
http://creativecommons.org/licenses/by/3.0/es
info:eu-repo/semantics/openAccess
rights_invalid_str_mv cc-by (c) Fernández Pérez, Francisco José et al., 2011
http://creativecommons.org/licenses/by/3.0/es
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv BioMed Central
publisher.none.fl_str_mv BioMed Central
dc.source.none.fl_str_mv Articles publicats en revistes (Bioquímica i Biomedicina Molecular)
reponame:Dipòsit Digital de la UB
instname:Universidad de Barcelona
instname_str Universidad de Barcelona
reponame_str Dipòsit Digital de la UB
collection Dipòsit Digital de la UB
repository.name.fl_str_mv
repository.mail.fl_str_mv
_version_ 1869410852628594688
score 15,300719

Similares en LA Referencia