Comparative Evolutionary Patterns of Burkholderia cenocepacia and B. multivorans During Chronic Co-infection of a Cystic Fibrosis Patient Lung
During chronic respiratory infections of cystic fibrosis (CF) patients, bacteria adaptively evolve in response to the nutritional and immune environment as well as influence other infecting microbes. The present study was designed to gain insights into the genetic mechanisms underlying adaptation an...
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doaj-c2d622e1cd2b4e12871bebc9b706af922020-11-25T01:59:39ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-09-011110.3389/fmicb.2020.574626574626Comparative Evolutionary Patterns of Burkholderia cenocepacia and B. multivorans During Chronic Co-infection of a Cystic Fibrosis Patient LungA. Amir Hassan0A. Amir Hassan1Sandra C. dos Santos2Vaughn S. Cooper3Isabel Sá-Correia4Isabel Sá-Correia5iBB - Institute for Bioengineering and Biosciences, Instituto Superior Técnico, Universidade de Lisboa, Lisbon, PortugalDepartment of Bioengineering, Instituto Superior Técnico, Universidade de Lisboa, Lisbon, PortugalDepartment of Bioengineering, Instituto Superior Técnico, Universidade de Lisboa, Lisbon, PortugalDepartment of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA, United StatesiBB - Institute for Bioengineering and Biosciences, Instituto Superior Técnico, Universidade de Lisboa, Lisbon, PortugalDepartment of Bioengineering, Instituto Superior Técnico, Universidade de Lisboa, Lisbon, PortugalDuring chronic respiratory infections of cystic fibrosis (CF) patients, bacteria adaptively evolve in response to the nutritional and immune environment as well as influence other infecting microbes. The present study was designed to gain insights into the genetic mechanisms underlying adaptation and diversification by the two most prevalent pathogenic species of the Burkholderia cepacia complex (Bcc), B. cenocepacia and B. multivorans. Herein, we study the evolution of both of these species during coinfection of a CF patient for 4.4 years using genome sequences of 9 B. multivorans and 11 B. cenocepacia. This co-infection spanned at least 3 years following initial infection by B. multivorans and ultimately ended in the patient’s death by cepacia syndrome. Both species acquired several mutations with accumulation rates of 2.08 (B. cenocepacia) and 2.27 (B. multivorans) SNPs/year. Many of the mutated genes are associated with oxidative stress response, transition metal metabolism, defense mechanisms against antibiotics, and other metabolic alterations consistent with the idea that positive selection might be driven by the action of the host immune system, antibiotic therapy and low oxygen and iron concentrations. Two orthologous genes shared by B. cenocepacia and B. multivorans were found to be under strong selection and accumulated mutations associated with lineage diversification. One gene encodes a nucleotide sugar dehydratase involved in lipopolysaccharide O-antigen (OAg) biosynthesis (wbiI). The other gene encodes a putative two-component regulatory sensor kinase protein required to sense and adapt to oxidative- and heavy metal- inducing stresses. This study contributes to understanding of shared and species-specific evolutionary patterns of B. cenocepacia and B. multivorans evolving in the same CF lung environment.https://www.frontiersin.org/article/10.3389/fmicb.2020.574626/fullBurkholderia cepacia complexcystic fibrosischronic pulmonary infectionswithin-host evolutioncomparative genomic analysisB. cenocepacia |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
A. Amir Hassan A. Amir Hassan Sandra C. dos Santos Vaughn S. Cooper Isabel Sá-Correia Isabel Sá-Correia |
spellingShingle |
A. Amir Hassan A. Amir Hassan Sandra C. dos Santos Vaughn S. Cooper Isabel Sá-Correia Isabel Sá-Correia Comparative Evolutionary Patterns of Burkholderia cenocepacia and B. multivorans During Chronic Co-infection of a Cystic Fibrosis Patient Lung Frontiers in Microbiology Burkholderia cepacia complex cystic fibrosis chronic pulmonary infections within-host evolution comparative genomic analysis B. cenocepacia |
author_facet |
A. Amir Hassan A. Amir Hassan Sandra C. dos Santos Vaughn S. Cooper Isabel Sá-Correia Isabel Sá-Correia |
author_sort |
A. Amir Hassan |
title |
Comparative Evolutionary Patterns of Burkholderia cenocepacia and B. multivorans During Chronic Co-infection of a Cystic Fibrosis Patient Lung |
title_short |
Comparative Evolutionary Patterns of Burkholderia cenocepacia and B. multivorans During Chronic Co-infection of a Cystic Fibrosis Patient Lung |
title_full |
Comparative Evolutionary Patterns of Burkholderia cenocepacia and B. multivorans During Chronic Co-infection of a Cystic Fibrosis Patient Lung |
title_fullStr |
Comparative Evolutionary Patterns of Burkholderia cenocepacia and B. multivorans During Chronic Co-infection of a Cystic Fibrosis Patient Lung |
title_full_unstemmed |
Comparative Evolutionary Patterns of Burkholderia cenocepacia and B. multivorans During Chronic Co-infection of a Cystic Fibrosis Patient Lung |
title_sort |
comparative evolutionary patterns of burkholderia cenocepacia and b. multivorans during chronic co-infection of a cystic fibrosis patient lung |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Microbiology |
issn |
1664-302X |
publishDate |
2020-09-01 |
description |
During chronic respiratory infections of cystic fibrosis (CF) patients, bacteria adaptively evolve in response to the nutritional and immune environment as well as influence other infecting microbes. The present study was designed to gain insights into the genetic mechanisms underlying adaptation and diversification by the two most prevalent pathogenic species of the Burkholderia cepacia complex (Bcc), B. cenocepacia and B. multivorans. Herein, we study the evolution of both of these species during coinfection of a CF patient for 4.4 years using genome sequences of 9 B. multivorans and 11 B. cenocepacia. This co-infection spanned at least 3 years following initial infection by B. multivorans and ultimately ended in the patient’s death by cepacia syndrome. Both species acquired several mutations with accumulation rates of 2.08 (B. cenocepacia) and 2.27 (B. multivorans) SNPs/year. Many of the mutated genes are associated with oxidative stress response, transition metal metabolism, defense mechanisms against antibiotics, and other metabolic alterations consistent with the idea that positive selection might be driven by the action of the host immune system, antibiotic therapy and low oxygen and iron concentrations. Two orthologous genes shared by B. cenocepacia and B. multivorans were found to be under strong selection and accumulated mutations associated with lineage diversification. One gene encodes a nucleotide sugar dehydratase involved in lipopolysaccharide O-antigen (OAg) biosynthesis (wbiI). The other gene encodes a putative two-component regulatory sensor kinase protein required to sense and adapt to oxidative- and heavy metal- inducing stresses. This study contributes to understanding of shared and species-specific evolutionary patterns of B. cenocepacia and B. multivorans evolving in the same CF lung environment. |
topic |
Burkholderia cepacia complex cystic fibrosis chronic pulmonary infections within-host evolution comparative genomic analysis B. cenocepacia |
url |
https://www.frontiersin.org/article/10.3389/fmicb.2020.574626/full |
work_keys_str_mv |
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