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Bacterial Infections

The uroS and yifB Genes Conserved among Tetrapyrrole Synthesizing-Deficient Bacteroidales Are Involved in Bacteroides fragilis Heme Assimilation and Survival in Experimental Intra-abdominal Infection and Intestinal Colonization

Anita C. Parker, Hector A. Bergonia, Nathaniel L. Seals, Cecile L. Baccanale, Edson R. Rocha
Andreas J. Bäumler, Editor
Anita C. Parker
aDepartment of Microbiology and Immunology, Brody School of Medicine, East Carolina University, Greenville, North Carolina, USA
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Hector A. Bergonia
bIron and Heme Core, Division of Hematology, University of Utah School of Medicine, Salt Lake City, Utah, USA
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Nathaniel L. Seals
aDepartment of Microbiology and Immunology, Brody School of Medicine, East Carolina University, Greenville, North Carolina, USA
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Cecile L. Baccanale
cDepartment of Comparative Medicine, Brody School of Medicine, East Carolina University, Greenville, North Carolina, USA
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Edson R. Rocha
aDepartment of Microbiology and Immunology, Brody School of Medicine, East Carolina University, Greenville, North Carolina, USA
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Andreas J. Bäumler
University of California, Davis
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DOI: 10.1128/IAI.00103-20
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ABSTRACT

The human intestinal anaerobic commensal and opportunistic pathogen Bacteroides fragilis does not synthesize the tetrapyrrole protoporphyrin IX in order to form heme that is required for growth stimulation and survival in vivo. Consequently, B. fragilis acquires essential heme from host tissues during extraintestinal infection. The absence of several genes necessary for de novo heme biosynthesis is a common characteristic of many anaerobic bacteria; however, the uroS gene, encoding a uroporphyrinogen III synthase for an early step of heme biosynthesis, is conserved among the heme-requiring Bacteroidales that inhabit the mammalian gastrointestinal tract. In this study, we show that the ability of B. fragilis to utilize heme or protoporphyrin IX for growth was greatly reduced in a ΔuroS mutant. This growth defect appears to be linked to the suppression of reverse chelatase and ferrochelatase activities in the absence of uroS. In addition, this ΔuroS suppressive effect was enhanced by the deletion of the yifB gene, which encodes an Mg2+-chelatase protein belonging to the ATPases associated with various cellular activities (AAA+) superfamily of proteins. Furthermore, the ΔuroS mutant and the ΔuroS ΔyifB double mutant had a severe survival defect compared to the parent strain in competitive infection assays using animal models of intra-abdominal infection and intestinal colonization. This shows that the presence of the uroS and yifB genes in B. fragilis seems to be linked to pathophysiological and nutritional competitive fitness for survival in host tissues. Genetic complementation studies and enzyme kinetics assays indicate that B. fragilis UroS is functionally different from canonical bacterial UroS proteins. Taken together, these findings show that heme assimilation and metabolism in the anaerobe B. fragilis have diverged from those of aerobic and facultative anaerobic pathogenic bacteria.

FOOTNOTES

    • Received 19 February 2020.
    • Returned for modification 4 March 2020.
    • Accepted 15 May 2020.
    • Accepted manuscript posted online 26 May 2020.
  • Supplemental material is available online only.

  • Copyright © 2020 American Society for Microbiology.

All Rights Reserved.

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The uroS and yifB Genes Conserved among Tetrapyrrole Synthesizing-Deficient Bacteroidales Are Involved in Bacteroides fragilis Heme Assimilation and Survival in Experimental Intra-abdominal Infection and Intestinal Colonization
Anita C. Parker, Hector A. Bergonia, Nathaniel L. Seals, Cecile L. Baccanale, Edson R. Rocha
Infection and Immunity Jul 2020, 88 (8) e00103-20; DOI: 10.1128/IAI.00103-20

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The uroS and yifB Genes Conserved among Tetrapyrrole Synthesizing-Deficient Bacteroidales Are Involved in Bacteroides fragilis Heme Assimilation and Survival in Experimental Intra-abdominal Infection and Intestinal Colonization
Anita C. Parker, Hector A. Bergonia, Nathaniel L. Seals, Cecile L. Baccanale, Edson R. Rocha
Infection and Immunity Jul 2020, 88 (8) e00103-20; DOI: 10.1128/IAI.00103-20
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KEYWORDS

Bacteroides fragilis
intestinal colonization
UroS
YifB
anaerobic infection
Ferrochelatase
heme assimilation
intra-abdominal infection
reverse chelatase
uroporphyrinogen III synthase

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