Bacterial Adaptation during Chronic Respiratory Infections

Chronic lung infections are associated with increased morbidity and mortality for individuals with underlying respiratory conditions such as cystic fibrosis (CF) and chronic obstructive pulmonary disease (COPD). The process of chronic colonisation allows pathogens to adapt over time to cope with changing selection pressures, co-infecting species and antimicrobial therapies. These adaptations can occur due to environmental pressures in the lung such as inflammatory responses, hypoxia, nutrient deficiency, osmolarity, low pH and antibiotic therapies. Phenotypic adaptations in bacterial pathogens from acute to chronic infection include, but are not limited to, antibiotic resistance, exopolysaccharide production (mucoidy), loss in motility, formation of small colony variants, increased mutation rate, quorum sensing and altered production of virulence factors associated with chronic infection. The evolution of Pseudomonas aeruginosa during chronic lung infection has been widely studied. More recently, the adaptations that other chronically colonising respiratory pathogens, including Staphylococcus aureus, Burkholderia cepacia complex and Haemophilus influenzae undergo during chronic infection have also been investigated. This review aims to examine the adaptations utilised by different bacterial pathogens to aid in their evolution from acute to chronic pathogens of the immunocompromised lung including CF and COPD.

[1]  S. Lewandowsky PLOS ONE 2013 , 2015 .

[2]  D. Speert,et al.  Swimming Motility in a Longitudinal Collection of Clinical Isolates of Burkholderia cepacia Complex Bacteria from People with Cystic Fibrosis , 2014, PloS one.

[3]  J. Curtis,et al.  Cell-associated bacteria in the human lung microbiome , 2014, Microbiome.

[4]  S. Molin,et al.  Within-Host Evolution of Pseudomonas aeruginosa Reveals Adaptation toward Iron Acquisition from Hemoglobin , 2014, mBio.

[5]  I. Sá-Correia,et al.  Burkholderia dolosa phenotypic variation during the decline in lung function of a cystic fibrosis patient during 5.5 years of chronic colonization. , 2014, Journal of medical microbiology.

[6]  A. Griffin,et al.  Loss of Social Behaviours in Populations of Pseudomonas aeruginosa Infecting Lungs of Patients with Cystic Fibrosis , 2014, PloS one.

[7]  Roy Kishony,et al.  Genetic variation of a bacterial pathogen within individuals with cystic fibrosis provides a record of selective pressures , 2013, Nature Genetics.

[8]  S. McClean,et al.  Proteomic Profiling of Burkholderia cenocepacia Clonal Isolates with Different Virulence Potential Retrieved from a Cystic Fibrosis Patient during Chronic Lung Infection , 2013, PloS one.

[9]  E. Marcotte,et al.  Pseudomonas aeruginosa Enhances Production of a Non-Alginate Exopolysaccharide during Long-Term Colonization of the Cystic Fibrosis Lung , 2013, PloS one.

[10]  Alexandro Rodríguez-Rojas,et al.  Antibiotics and antibiotic resistance: a bitter fight against evolution. , 2013, International journal of medical microbiology : IJMM.

[11]  H. Dienemann,et al.  Analysis of the Airway Microbiota of Healthy Individuals and Patients with Chronic Obstructive Pulmonary Disease by T-RFLP and Clone Sequencing , 2013, PloS one.

[12]  J. Harris,et al.  Inflammation and Airway Microbiota during Cystic Fibrosis Pulmonary Exacerbations , 2013, PloS one.

[13]  M. Surette,et al.  Phenotypic Heterogeneity of Pseudomonas aeruginosa Populations in a Cystic Fibrosis Patient , 2013, PloS one.

[14]  B. Berwin,et al.  Flagellar Motility Is a Key Determinant of the Magnitude of the Inflammasome Response to Pseudomonas aeruginosa , 2013, Infection and Immunity.

[15]  L. Amaral,et al.  Mechanisms of Resistance in Bacteria: An Evolutionary Approach , 2013, The open microbiology journal.

[16]  T. Coenye,et al.  Phenotypic and Genotypic Characterisation of Burkholderia cenocepacia J2315 Mutants Affected in Homoserine Lactone and Diffusible Signal Factor-Based Quorum Sensing Systems Suggests Interplay between Both Types of Systems , 2013, PloS one.

[17]  G. Rogers,et al.  Impact of antibiotic treatment for pulmonary exacerbations on bacterial diversity in cystic fibrosis. , 2013, Journal of cystic fibrosis : official journal of the European Cystic Fibrosis Society.

[18]  J. Vazquez,et al.  Development and antimicrobial susceptibility studies of in vitro monomicrobial and polymicrobial biofilm models with Aspergillus fumigatus and Pseudomonas aeruginosa , 2014, BMC Microbiology.

[19]  V. Cooper,et al.  Tangled bank of experimentally evolved Burkholderia biofilms reflects selection during chronic infections , 2012, Proceedings of the National Academy of Sciences.

[20]  Anders Folkesson,et al.  Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective , 2012, Nature Reviews Microbiology.

[21]  S. McClean,et al.  Immunoproteomics: The Key to Discovery of New Vaccine Antigens Against Bacterial Respiratory Infections , 2012, Current protein & peptide science.

[22]  Jenny Renaut,et al.  Gel-Based and Gel-Free Quantitative Proteomics Approaches at a Glance , 2012, International journal of plant genomics.

[23]  V. Young,et al.  The microbiome of the lung. , 2012, Translational research : the journal of laboratory and clinical medicine.

[24]  S. McClean Eight stranded -Barrel and Related Outer Membrane Proteins: Role in Bacterial Pathogenesis , 2017 .

[25]  W. Morgan,et al.  Multiple antibiotic-resistant Pseudomonas aeruginosa and lung function decline in patients with cystic fibrosis. , 2012, Journal of cystic fibrosis : official journal of the European Cystic Fibrosis Society.

[26]  Sam P. Brown,et al.  Evolution of virulence in opportunistic pathogens: generalism, plasticity, and control , 2012, Trends in microbiology.

[27]  S. Leroy,et al.  The Airway Microbiota in Cystic Fibrosis: A Complex Fungal and Bacterial Community—Implications for Therapeutic Management , 2012, PloS one.

[28]  G. Khanbabaee,et al.  A survey on pulmonary pathogens and their antibiotic susceptibility among cystic fibrosis patients. , 2012, The Brazilian journal of infectious diseases : an official publication of the Brazilian Society of Infectious Diseases.

[29]  S. McClean,et al.  Bacterial host interactions in cystic fibrosis. , 2012, Current opinion in microbiology.

[30]  I. Sá-Correia,et al.  Genomic Expression Analysis Reveals Strategies of Burkholderia cenocepacia to Adapt to Cystic Fibrosis Patients' Airways and Antimicrobial Therapy , 2011, PloS one.

[31]  J. Becker,et al.  Mucoid morphotype variation of Burkholderia multivorans during chronic cystic fibrosis lung infection is correlated with changes in metabolism, motility, biofilm formation and virulence. , 2011, Microbiology.

[32]  Kyle Bittinger,et al.  Topographical continuity of bacterial populations in the healthy human respiratory tract. , 2011, American journal of respiratory and critical care medicine.

[33]  Deborah M Anderson,et al.  Host Defense and the Airway Epithelium: Frontline Responses That Protect against Bacterial Invasion and Pneumonia , 2011, Journal of pathogens.

[34]  K. Templeton,et al.  Adaptive Evolution of Staphylococcus aureus during Chronic Endobronchial Infection of a Cystic Fibrosis Patient , 2011, PloS one.

[35]  C. Goss,et al.  Review: Staphylococcus aureus and MRSA in cystic fibrosis. , 2011, Journal of cystic fibrosis : official journal of the European Cystic Fibrosis Society.

[36]  Lars Jelsbak,et al.  Bacterial adaptation during chronic infection revealed by independent component analysis of transcriptomic data , 2011, BMC Microbiology.

[37]  P. Sokol,et al.  Burkholderia cenocepacia ShvR-Regulated Genes That Influence Colony Morphology, Biofilm Formation, and Virulence , 2011, Infection and Immunity.

[38]  S. Nseir,et al.  Short term Candida albicans colonization reduces Pseudomonas aeruginosa-related lung injury and bacterial burden in a murine model , 2011, Critical care.

[39]  Tao Liu,et al.  Liquid Chromatography-Mass Spectrometry-based Quantitative Proteomics* , 2011, The Journal of Biological Chemistry.

[40]  Carla C. C. R. de Carvalho,et al.  Burkholderia cenocepacia Phenotypic Clonal Variation during a 3.5-Year Colonization in the Lungs of a Cystic Fibrosis Patient , 2011, Infection and Immunity.

[41]  Anders Folkesson,et al.  Evolutionary dynamics of bacteria in a human host environment , 2011, Proceedings of the National Academy of Sciences.

[42]  I. Sá-Correia,et al.  Quantitative proteomics (2‐D DIGE) reveals molecular strategies employed by Burkholderia cenocepacia to adapt to the airways of cystic fibrosis patients under antimicrobial therapy , 2011, Proteomics.

[43]  J. Curtis,et al.  Analysis of the Lung Microbiome in the “Healthy” Smoker and in COPD , 2011, PloS one.

[44]  S. McKeon,et al.  Functional quorum sensing systems are maintained during chronic Burkholderia cepacia complex infections in patients with cystic fibrosis. , 2011, The Journal of infectious diseases.

[45]  R. Proctor,et al.  Staphylococcus aureus phenotype switching: an effective bacterial strategy to escape host immune response and establish a chronic infection , 2011, EMBO molecular medicine.

[46]  A. Fodor,et al.  Use of culture and molecular analysis to determine the effect of antibiotic treatment on microbial community diversity and abundance during exacerbation in patients with cystic fibrosis , 2011, Thorax.

[47]  S. McColley,et al.  Clinical Significance of Microbial Infection and Adaptation in Cystic Fibrosis , 2011, Clinical Microbiology Reviews.

[48]  J. Gilsdorf,et al.  Molecular Basis of Increased Serum Resistance among Pulmonary Isolates of Non-typeable Haemophilus influenzae , 2011, PLoS pathogens.

[49]  R. Brant,et al.  Mucoid and nonmucoid Burkholderia cepacia complex bacteria in cystic fibrosis infections. , 2011, American journal of respiratory and critical care medicine.

[50]  A. Oliver Mutators in cystic fibrosis chronic lung infection: Prevalence, mechanisms, and consequences for antimicrobial therapy. , 2010, International journal of medical microbiology : IJMM.

[51]  J. Heesemann,et al.  Adaptation of Pseudomonas aeruginosa during persistence in the cystic fibrosis lung. , 2010, International journal of medical microbiology : IJMM.

[52]  Gordon Ramage,et al.  Pseudomonas aeruginosa and their small diffusible extracellular molecules inhibit Aspergillus fumigatus biofilm formation. , 2010, FEMS microbiology letters.

[53]  L. Nicod,et al.  [Pseudomonas aeruginosa in chronic obstructive pulmonary disease]. , 2010, Revue medicale suisse.

[54]  T. Welte,et al.  Antimicrobial treatment of nosocomial meticillin-resistant Staphylococcus aureus (MRSA) pneumonia: current and future options. , 2010, International journal of antimicrobial agents.

[55]  D. Viemann,et al.  Staphylococcus aureus small-colony variants are adapted phenotypes for intracellular persistence. , 2010, The Journal of infectious diseases.

[56]  D. Speert,et al.  The role of mucoidy in virulence of bacteria from the Burkholderia cepacia complex: a systematic proteomic and transcriptomic analysis. , 2010, The Journal of infectious diseases.

[57]  Jason A. Papin,et al.  Metabolic Network Analysis of Pseudomonas aeruginosa during Chronic Cystic Fibrosis Lung Infection , 2010, Journal of bacteriology.

[58]  M. Valvano,et al.  A Decade of Burkholderia cenocepacia Virulence Determinant Research , 2010, Infection and Immunity.

[59]  Eoin L. Brodie,et al.  Airway Microbiota and Pathogen Abundance in Age-Stratified Cystic Fibrosis Patients , 2010, PloS one.

[60]  J. Fothergill,et al.  Fluctuations in phenotypes and genotypes within populations of Pseudomonas aeruginosa in the cystic fibrosis lung during pulmonary exacerbations. , 2010, Journal of medical microbiology.

[61]  Lior Pachter,et al.  Disordered Microbial Communities in Asthmatic Airways , 2010, PloS one.

[62]  B. Tümmler,et al.  Pseudomonas aeruginosa population biology in chronic obstructive pulmonary disease. , 2009, The Journal of infectious diseases.

[63]  S. Nseir,et al.  Management of invasive aspergillosis in patients with COPD: Rational use of voriconazole , 2009, International journal of chronic obstructive pulmonary disease.

[64]  T. Voyno-Yasenetskaya,et al.  Lipopolysaccharide Stimulates Platelet Secretion and Potentiates Platelet Aggregation via TLR4/MyD88 and the cGMP-Dependent Protein Kinase Pathway1 , 2009, The Journal of Immunology.

[65]  B. Rubin Mucus, phlegm, and sputum in cystic fibrosis. , 2009, Respiratory care.

[66]  Matthew R. Parsek,et al.  Pseudomonas aeruginosa Rugose Small-Colony Variants Have Adaptations That Likely Promote Persistence in the Cystic Fibrosis Lung , 2009, Journal of bacteriology.

[67]  P. François,et al.  CodY in Staphylococcus aureus: a Regulatory Link between Metabolism and Virulence Gene Expression , 2009, Journal of bacteriology.

[68]  G. Amoutzias,et al.  Role of siderophores in cystic fibrosis pathogenesis: foes or friends? , 2009, International journal of medical microbiology : IJMM.

[69]  S. Molin,et al.  Novel experimental Pseudomonas aeruginosa lung infection model mimicking long-term host–pathogen interactions in cystic fibrosis , 2009, APMIS : acta pathologica, microbiologica, et immunologica Scandinavica.

[70]  M. Maciá,et al.  Chronic Pseudomonas aeruginosa infection in chronic obstructive pulmonary disease. , 2008, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[71]  S. Quirce,et al.  Aspergillus fumigatus y Candida albicans en la fibrosis quística: significado clínico e inmunorrespuestas séricas específicas de inmunoglobulinas G, A y M , 2008 .

[72]  L. M. Moreira,et al.  Differential Mucoid Exopolysaccharide Production by Members of the Burkholderia cepacia Complex , 2008, Journal of Clinical Microbiology.

[73]  A. H. Wang,et al.  Discovery of virulence factors of pathogenic bacteria. , 2008, Current opinion in chemical biology.

[74]  S. Quirce,et al.  [Aspergillus fumigatus and Candida albicans in cystic fibrosis: clinical significance and specific immune response involving serum immunoglobulins G, A, and M]. , 2008, Archivos de bronconeumologia.

[75]  Steve P. Bernier,et al.  A LysR-Type Transcriptional Regulator in Burkholderia cenocepacia Influences Colony Morphology and Virulence , 2007, Infection and Immunity.

[76]  M. Parsek,et al.  Pseudomonas aeruginosa Psl Is a Galactose- and Mannose-Rich Exopolysaccharide , 2007, Journal of bacteriology.

[77]  F. Zanetti,et al.  Exopolysaccharides produced by clinical strains belonging to the Burkholderia cepacia complex. , 2007, Journal of cystic fibrosis : official journal of the European Cystic Fibrosis Society.

[78]  David A. D'Argenio,et al.  Growth phenotypes of Pseudomonas aeruginosa lasR mutants adapted to the airways of cystic fibrosis patients , 2007, Molecular microbiology.

[79]  S. Levy,et al.  Molecular Mechanisms of Antibacterial Multidrug Resistance , 2007, Cell.

[80]  S. Johnston,et al.  The role of antibiotics in asthma , 2007, International Journal of Antimicrobial Agents.

[81]  F. Blasi,et al.  Antibiotic therapy and prophylaxis in COPD , 2007 .

[82]  J. Shiloach,et al.  A perspective on microarrays: current applications, pitfalls, and potential uses , 2007, Microbial cell factories.

[83]  R. Boucher,et al.  Evidence for airway surface dehydration as the initiating event in CF airway disease , 2007, Journal of internal medicine.

[84]  D. Speert,et al.  Proteomic identification and characterization of bacterial factors associated with Burkholderia cenocepacia survival in a murine host. , 2007, Microbiology.

[85]  J. Heesemann,et al.  Stage-specific adaptation of hypermutable Pseudomonas aeruginosa isolates during chronic pulmonary infection in patients with cystic fibrosis. , 2007, The Journal of infectious diseases.

[86]  L. Saiman,et al.  Antimicrobial Susceptibility and Synergy Studies of Burkholderia cepacia Complex Isolated from Patients with Cystic Fibrosis , 2006, Antimicrobial Agents and Chemotherapy.

[87]  Pradeep K. Singh,et al.  Evolving stealth: genetic adaptation of Pseudomonas aeruginosa during cystic fibrosis infections. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[88]  David A. D'Argenio,et al.  Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[89]  M. Otto,et al.  Staphylococcus quorum sensing in biofilm formation and infection. , 2006, International journal of medical microbiology : IJMM.

[90]  A. S. Lynch Efflux systems in bacterial pathogens: an opportunity for therapeutic intervention? An industry view. , 2006, Biochemical pharmacology.

[91]  R. Ernst,et al.  Exopolysaccharides from Burkholderia cenocepacia Inhibit Neutrophil Chemotaxis and Scavenge Reactive Oxygen Species* , 2006, Journal of Biological Chemistry.

[92]  M. Denton,et al.  Staphylococcus aureus and MRSA , 2006 .

[93]  A. Alanis,et al.  Resistance to antibiotics: are we in the post-antibiotic era? , 2005, Archives of medical research.

[94]  Matthew R. Parsek,et al.  Characterization of Colony Morphology Variants Isolated from Pseudomonas aeruginosa Biofilms , 2005, Applied and Environmental Microbiology.

[95]  B. Grant,et al.  Moraxella catarrhalis in chronic obstructive pulmonary disease: burden of disease and immune response. , 2005, American journal of respiratory and critical care medicine.

[96]  F. Pattus,et al.  The Crystal Structure of the Pyoverdine Outer Membrane Receptor FpvA from Pseudomonas aeruginosa at 3.6 Å Resolution , 2005 .

[97]  M. Freeman,et al.  Distinct Roles of Pattern Recognition Receptors CD14 and Toll-Like Receptor 4 in Acute Lung Injury , 2005, Infection and Immunity.

[98]  S. Rennard,et al.  Pathogenesis of COPD. , 2003, Clinical cornerstone.

[99]  F. Pattus,et al.  The crystal structure of the pyoverdine outer membrane receptor FpvA from Pseudomonas aeruginosa at 3.6 angstroms resolution. , 2005, Journal of molecular biology.

[100]  C. Wolz,et al.  Regulatory and genomic plasticity of Staphylococcus aureus during persistent colonization and infection. , 2004, International journal of medical microbiology : IJMM.

[101]  Michael E. Watson,et al.  Hypermutable Haemophilus influenzae with mutations in mutS are found in cystic fibrosis sputum. , 2004, Microbiology.

[102]  J. Buer,et al.  Expression Analysis of a Highly Adherent and Cytotoxic Small Colony Variant of Pseudomonas aeruginosa Isolated from a Lung of a Patient with Cystic Fibrosis , 2004, Journal of bacteriology.

[103]  S. Majumdar,et al.  Importance of the Ornibactin and Pyochelin Siderophore Transport Systems in Burkholderia cenocepacia Lung Infections , 2004, Infection and Immunity.

[104]  Herbert Schmidt,et al.  Pathogenicity Islands in Bacterial Pathogenesis , 2004, Clinical Microbiology Reviews.

[105]  S. Häussler,et al.  Evaluation of the Merlin, Micronaut System for Automated Antimicrobial Susceptibility Testing of Pseudomonas aeruginosa and Burkholderia Species Isolated from Cystic Fibrosis Patients , 2003, European Journal of Clinical Microbiology and Infectious Diseases.

[106]  S. M. Kirov Bacteria that express lateral flagella enable dissection of the multifunctional roles of flagella in pathogenesis. , 2003, FEMS microbiology letters.

[107]  P. Vandamme,et al.  Fatal Outcome of Lung Transplantation in Cystic Fibrosis Patients due to Small-Colony Variants of the Burkholderia cepacia Complex , 2003, European Journal of Clinical Microbiology and Infectious Diseases.

[108]  J. Bargon,et al.  Prevalence of Aspergillus fumigatus and other fungal species in the sputum of adult patients with cystic fibrosis , 2003, Mycoses.

[109]  T. Beveridge,et al.  Colonial Morphology of Burkholderia cepacia Complex Genomovar III: Implications in Exopolysaccharide Production, Pilus Expression, and Persistence in the Mouse , 2003, Infection and Immunity.

[110]  H. Sahl,et al.  Mutations are involved in emergence of aminoglycoside-induced small colony variants of Staphylococcus aureus. , 2003, International journal of medical microbiology : IJMM.

[111]  J. Musser,et al.  Evolutionary genomics of pathogenic bacteria. , 2001, Trends in microbiology.

[112]  D. Metze,et al.  Intracellular persistence of Staphylococcus aureus small-colony variants within keratinocytes: a cause for antibiotic treatment failure in a patient with darier's disease. , 2001, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[113]  K. Mathee,et al.  Posttranslational control of the algT (algU)-encoded sigma22 for expression of the alginate regulon in Pseudomonas aeruginosa and localization of its antagonist proteins MucA and MucB (AlgN) , 1997, Journal of bacteriology.

[114]  R. Proctor,et al.  Decreased susceptibility to antibiotic killing of a stable small colony variant of Staphylococcus aureus in fluid phase and on fibronectin-coated surfaces. , 1997, The Journal of antimicrobial chemotherapy.

[115]  V. Deretic,et al.  Microbial pathogenesis in cystic fibrosis: co‐ordinate regulation of heat‐shock response and conversion to mucoidy in Pseudomonas aeruginosa , 1997, Molecular microbiology.

[116]  V. Deretic,et al.  Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. , 1996, Microbiological reviews.

[117]  V. Deretic,et al.  Control of AlgU, a member of the sigma E-like family of stress sigma factors, by the negative regulators MucA and MucB and Pseudomonas aeruginosa conversion to mucoidy in cystic fibrosis , 1996, Journal of bacteriology.

[118]  R. Proctor,et al.  Gentamicin-resistant menadione and hemin auxotrophic Staphylococcus aureus persist within cultured endothelial cells. , 1994, The Journal of infectious diseases.

[119]  E. Mahenthiralingam,et al.  Nonmotility and phagocytic resistance of Pseudomonas aeruginosa isolates from chronically colonized patients with cystic fibrosis , 1994, Infection and immunity.

[120]  D. Martin,et al.  Mechanism of conversion to mucoidy in Pseudomonas aeruginosa infecting cystic fibrosis patients. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[121]  P. Libby,et al.  Cytokine induction by lipopolysaccharide (LPS) corresponds to lethal toxicity and is inhibited by nontoxic Rhodobacter capsulatus LPS , 1990, Infection and immunity.

[122]  Y. Ogawa,et al.  Involvement of central action of lipopolysaccharide in pyrogen fever. , 1984, Japanese journal of pharmacology.

[123]  R. Hancock,et al.  Pseudomonas aeruginosa isolates from patients with cystic fibrosis: a class of serum-sensitive, nontypable strains deficient in lipopolysaccharide O side chains , 1983, Infection and immunity.

[124]  R. Jones,et al.  A new polysaccharide resembling alginic acid isolated from pseudomonads. , 1966, The Journal of biological chemistry.