The hmuQ and hmuD Genes from Bradyrhizobium japonicum Encode Heme-Degrading Enzymes

Puri, Sumant; O'Brian, Mark R.

doi:10.1128/jb.00737-06

Cited by 59Hemoglobin structure and functionHeme Oxygenase-1 and Carbon MonoxideMetal-Catalyzed Oxygenation Mechanisms

The hmuQ and hmuD Genes from Bradyrhizobium japonicum Encode Heme-Degrading Enzymes

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Puri, Sumant, O'Brian, Mark R.·2006·Journal of Bacteriology

DOI 10.1128/jb.00737-06PMC PMC1595471

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Abstract

Utilization of heme by bacteria as a nutritional iron source involves the transport of exogenous heme, followed by cleavage of the heme macrocycle to release iron. Bradyrhizobium japonicum can use heme as an iron source, but no heme-degrading oxygenase has been described. Here, bioinformatics analyses of the B. japonicum genome identified two paralogous genes renamed hmuQ (bll7075) and hmuD (bll7423) that encode proteins with weak similarity to the heme-degrading monooxygenase IsdG from Staphylococcus aureus. The hmuQ gene is clustered with known heme transport genes in the genome. Recombinant HmuQ bound heme with a K(d) value of 0.8 microM and showed spectral properties consistent with a heme oxygenase. In the presence of a reductant, HmuQ catalyzed the degradation of heme and the formation of biliverdin. The hmuQ and hmuD genes complemented a Corynebacterium ulcerans heme oxygenase mutant in trans for utilization of heme as the sole iron source for growth. Furthermore, homologs of hmuQ and hmuD were identified in many bacterial genera, and the recombinant homolog from Brucella melitensis bound heme and catalyzed its degradation. The findings show that hmuQ and hmuD encode heme oxygenases and indicate that the IsdG family of heme-degrading monooxygenases is not restricted to gram-positive pathogenic bacteria.

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IsdG orthologs from these bacteria bind and degrade heme, but they differ in other respects.
“While IsdG orthologs from each of these bacteria have been shown to bind and degrade heme, differences do exist.”
From A battle for iron: host sequestration and Staphylococcus aureus acquisition (2012) · cites this paper as [57]
IsdG-family heme oxygenases have been characterized in S. lugdunensis, Bacillus anthracis, Bradyrhizobium japonicum, Brucella melitensis, and Mycobacterium tuberculosis.
“IsdG-family heme oxygenases have been characterized in S. lugdunensis, Bacillus anthracis, Bradyrhizobium japonicum, Brucella melitensis, and Mycobacterium tuberculosis [46, 50, 56–58].”
From A battle for iron: host sequestration and Staphylococcus aureus acquisition (2012) · cites this paper as [57]

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“Heme binding by PefR was assessed spectroscopically as described in Puri and O’brian (2006) and Ouattara et al. (2010) with minor modifications.”
Method
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BackgroundMethodInfluential
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“Interestingly, other heme degrading enzymes are present in some bacteria that show no sequence and structural similarity to known HOs (Skaar et al. 2004; Puri and O’Brian 2006).”
Background
The affinity of MhuD for heme is consistent with a heme degrading functionin vivo
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“Other members of the IsdG HO family include HmuD and HmuQ from Bradyrhizobium japonicum (Puri and O’Brian 2006), IsdG homologues from Bacillus anthracis (Skaar et al. 2006) and S. lugdunensis (Haley et al. 2011).”
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Influential
The bhuTUV and bhuO genes play vital roles in the ability of Brucella abortus to use heme as an iron source and are regulated in an iron-responsive manner by RirA and Irr
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Heme Degradation as Catalyzed by a Recombinant Bacterial Heme Oxygenase (Hmu O) from Corynebacterium diphtheriae
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The bhuQ Gene Encodes a Heme Oxygenase That Contributes to the Ability of Brucella abortus 2308 To Use Heme as an Iron Source and Is Regulated by Irr
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Authors: Puri, S., & O'Brian, M. R.
Affiliations: University at Buffalo, State University of New York (US)
Department of Biochemistry and Witebsky Center for Microbial Pathogenesis and Immunology, State University of New York at Buffalo, Buffalo, New York
ORCID: Puri, Sumant
Venue: Journal of Bacteriology
Publisher: American Society for Microbiology
Published: 2006-09-15
Volume: 188
Issue: 18
Pages: 6476-6482
ISSN: 0021-9193 (ISSN-L)
1098-5530
DOI: 10.1128/jb.00737-06
PMC: PMC1595471
OpenAlex: W1979033093
Cited by: 59
References: 35
Citations by year: 2025: 1 · 2024: 2 · 2023: 1 · 2022: 3 · 2019: 3 · 2018: 1 · 2017: 2 · 2016: 3 · 2015: 1 · 2014: 4 · 2013: 5 · 2012: 10
FWCI: 1.80
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Journal of Bacteriology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Institute of General Medical Sciences (R01GM067966)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Hemoglobin structure and function
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heme Oxygenase-1 and Carbon Monoxide
Physical Sciences › Chemistry › Inorganic Chemistry › Metal-Catalyzed Oxygenation Mechanisms
Keywords: Bradyrhizobium japonicum, heme oxygenase, heme utilization, iron acquisition, biliverdin, gene complementation, Corynebacterium ulcerans, Brucella melitensis
MeSH terms: Amino Acid Sequence, Bacterial Proteins, Biliverdine, Corynebacterium, Genes, Bacterial, Multigene Family, Genetic Complementation Test, Heme, Mixed Function Oxygenases, Molecular Sequence Data, Protein Binding, Recombinant Proteins, Spectrum Analysis, Staphylococcus aureus, Genome, Bacterial, Brucella melitensis, Sequence Homology, Amino Acid, Computational Biology, Bradyrhizobium

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The hmuQ and hmuD Genes from Bradyrhizobium japonicum Encode Heme-Degrading Enzymes

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