Epigenetic control of the ferric uptake regulator (Fur) and fumarate nitrate reductase (FNR) master regulatory proteins contributes to Haemophilus influenzae survival during lung infection

DNA regulatory elements that dictate how the bacterial pathobiont Haemophilus influenzae infects and adapts to the airways of immunocompromised patients suffering from chronic obstructive pulmonary disease (COPD) are poorly understood. This is in part due to the scarcity of research integrating gene...

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Detalles Bibliográficos
Autores: Gil-Campillo, Celia, Euba, Begoña, Rodríguez-Arce, Irene, San León, David, Marino, Mary C., Asensio-López, Javier, Gutiérrez Pozo, Gabriel, Sánchez Romero, María Antonia, Garmendia, Junkal
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2025
País:España
Institución:Universidad de Sevilla (US)
Repositorio:idUS. Depósito de Investigación de la Universidad de Sevilla
OAI Identifier:oai:idus.us.es:11441/180495
Acceso en línea:https://hdl.handle.net/11441/180495
https://doi.org/10.1128/mbio.01355-25
Access Level:acceso abierto
Palabra clave:Haemophilus influenzae
In vivo Tn-seq
Airway infection
Epigenetic regulation of gene expression
DNA adenine Dam methylation
FNR regulon
Fur regulation
Gene expression heterogeneity
Descripción
Sumario:DNA regulatory elements that dictate how the bacterial pathobiont Haemophilus influenzae infects and adapts to the airways of immunocompromised patients suffering from chronic obstructive pulmonary disease (COPD) are poorly understood. This is in part due to the scarcity of research integrating genetic and epigenetic perspectives to shed light on the role of distinct bacterial adaptive strategies within the human airways. In this work, global fitness profilingof H. influenzae mutants by high-throughput transposon mutant sequencing within the mouse lung identified Dam methyltransferase as an in vivo requirement for respiratory infection. Equally, single-molecule real-time sequencing methylome analyses found undermethylation of GATC motifs within putative regulatory elements and revealed the first case of phenotypic variation controlled by variable Dam methylation in H. influenzae. Moreover, RNA sequencing differentialgene expression disclosed a novel regulatory network where Dam methyltransferase positively regulates the expression of the ferric uptake regulator (Fur), which in turn represses the expression of the fumarate nitrate reductase (FNR) regulator and, subsequently, of a repertoire of genes that belong to the FNR regulon and encode bacterial anaerobic defenses against, among others, reactive nitrogen species produced within the diseased airways. Our results present a multifactorial regulatory network where the interplay between the Fur and FNR master transcriptional regulators is controlled epigenetically by Dam methylation. We put forward the notion that this network regulates H. influenzae survival in diseased airway niches with high nitrosative stress where damage reduces the amount of oxygen in the lungs, as encountered in COPD.