Nitric oxide scavenging and detoxification by the Mycobacterium tuberculosis haemoglobin, HbN in Escherichia coli

Mol Microbiol. 2002 Sep;45(5):1303-14. doi: 10.1046/j.1365-2958.2002.03095.x.

Abstract

Nitric oxide (NO), generated in large amounts within the macrophages, controls and restricts the growth of internalized human pathogen, Mycobacterium tuberculosis H37Rv. The molecular mechanism by which tubercle bacilli survive within macrophages is currently of intense interest. In this work, we have demonstrated that dimeric haemoglobin, HbN, from M. tuberculosis exhibits distinct nitric oxide dioxygenase (NOD) activity and protects growth and cellular respiration of heterologous hosts, Escherichia coli and Mycobacterium smegmatis, from the toxic effect of exogenous NO and the NO-releasing compounds. A flavohaemoglobin (HMP)-deficient mutant of E. coli, unable to metabolize NO, acquired an oxygen-dependent NO consumption activity in the presence of HbN. On the basis of cellular haem content, the specific NOD activity of HbN was nearly 35-fold higher than the single-domain Vitreoscilla haemoglobin (VHb) but was sevenfold lower than the two-domain flavohaemoglobin. HbN-dependent NO consumption was sustained with repeated addition of NO, demonstrating that HbN is catalytically reduced within E. coli. Aerobic growth and respiration of a flavohaemoglobin (HMP) mutant of E. coli was inhibited in the presence of exogenous NO but remained insensitive to NO inhibition when these cells produced HbN, VHb or flavohaemoglobin. M. smegmatis, carrying a native HbN very similar to M. tuberculosis HbN, exhibited a 7.5-fold increase in NO uptake when exposed to gaseous NO, suggesting NO-induced NOD activity in these cells. In addition, expression of plasmid-encoded HbN of M. tuberculosis in M. smegmatis resulted in 100-fold higher NO consumption activity than the isogenic control cells. These results provide strong experimental evidence in support of NO scavenging and detoxification function for the M. tuberculosis HbN. The catalytic NO scavenging by HbN may be highly advantageous for the survival of tubercle bacilli during infection and pathogenesis.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Amino Acid Sequence
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Base Sequence
  • DNA, Bacterial / genetics
  • Dihydropteridine Reductase*
  • Escherichia coli / genetics
  • Escherichia coli / growth & development
  • Escherichia coli / metabolism*
  • Escherichia coli Proteins / genetics
  • Escherichia coli Proteins / metabolism
  • Genes, Bacterial
  • Hemeproteins / genetics
  • Hemeproteins / metabolism
  • Hemoglobins / chemistry
  • Hemoglobins / genetics
  • Hemoglobins / metabolism*
  • Humans
  • Molecular Sequence Data
  • Mutation
  • Mycobacterium smegmatis / genetics
  • Mycobacterium smegmatis / growth & development
  • Mycobacterium smegmatis / metabolism
  • Mycobacterium tuberculosis / genetics
  • Mycobacterium tuberculosis / metabolism*
  • NADH, NADPH Oxidoreductases*
  • Nitric Oxide / metabolism*
  • Oxygen Consumption
  • Oxygenases / genetics
  • Oxygenases / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Sequence Homology, Amino Acid
  • Truncated Hemoglobins

Substances

  • Bacterial Proteins
  • DNA, Bacterial
  • Escherichia coli Proteins
  • Hemeproteins
  • Hemoglobins
  • Recombinant Proteins
  • Truncated Hemoglobins
  • hemoglobin protein, Vitreoscilla
  • Nitric Oxide
  • Oxygenases
  • flavohemoglobin denitrosylase
  • Dihydropteridine Reductase
  • hmp protein, E coli
  • NADH, NADPH Oxidoreductases