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Title: Differential Regulation of the Two Ferrochelatase Paralogues in Shewanella loihica PV-4 in Response to Environmental Stresses

Determining the function and regulation of paralogues is important in understanding microbial functional genomics and environmental adaptation. Heme homeostasis is crucial for the survival of environmental microorganisms. MostShewanellaspecies encode two paralogues of ferrochelatase, the terminal enzyme in the heme biosynthesis pathway. The function and transcriptional regulation of two ferrochelatase genes, hemH1 and hemH2, were investigated inShewanellaloihicaPV-4. The disruption of hemH1 but not hemH2 resulted in a significant accumulation of extracellular protoporphyrin IX (PPIX), the precursor to heme, and decreased intracellular heme levels.hemH1 was constitutively expressed, and the expression of hemH2 increased when hemH1 was disrupted. The transcription ofhemH1was regulated by the housekeeping sigma factor RpoD and potentially regulated by OxyR, while hemH2 appeared to be regulated by the oxidative stress-associated sigma factor RpoE2. When an oxidative stress condition was mimicked by adding H 2O 2 to the medium or exposing the culture to light, PPIX accumulation was suppressed in the Δ hemH1 mutant. Consistently, transcriptome analysis indicated enhanced iron uptake and suppressed heme synthesis in the ΔhemH1 mutant. These data indicate that the two paralogues are functional in the heme synthesis pathway but regulated by environmental conditions, providing insights into the understanding of bacterial response to environmental stresses and amore » great potential to commercially produce porphyrin compounds.Shewanella is capable of utilizing a variety of electron acceptors for anaerobic respiration because of the existence of multiple c -type cytochromes in which heme is an essential component. The cytochrome-mediated electron transfer across cellular membranes could potentially be used for biotechnological purposes, such as electricity generation in microbial fuel cells and dye decolorization. However, the mechanism underlying the regulation of biosynthesis of heme and cytochromes is poorly understood. In conclusion, our study has demonstrated that two ferrochelatase genes involved in heme biosynthesis are differentially regulated in response to environmental stresses, including light and reactive oxygen species. This is an excellent example showing how bacteria have evolved to maintain cellular heme homeostasis. More interestingly, the high yields of extracellular protoporphyrin IX by theShewanella loihicaPV-4 mutants could be utilized for commercial production of this valuable chemical via bacterial fermentation.« less
Authors:
 [1] ;  [2] ;  [3] ;  [3] ;  [3] ;  [4] ;  [2] ;  [2] ;  [2] ;  [5] ;  [6]
  1. Chinese Academy of Sciences (CAS), Wuhan (China). Inst. of Hydrobiology; Univ. of Chinese Academy of Sciences, Beijing (China); Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics, Dept. of Microbiology and Plant Biology
  2. Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics, Dept. of Microbiology and Plant Biology
  3. Chinese Academy of Sciences (CAS), Wuhan (China). Inst. of Hydrobiology; Univ. of Chinese Academy of Sciences, Beijing (China)
  4. Hubei Engineering Univ., Xiaogan (China). School of Life Sciences and Technology
  5. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Earth Science Division
  6. Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics, Dept. of Microbiology and Plant Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth Science Division; Tsinghua Univ., Beijing (China). State Key Joint Lab. of Environment Simulation and Pollution Control, School of Environment
Publication Date:
Grant/Contract Number:
AC02-05CH11231; FG02-07ER64383; Y15103-1-401
Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 82; Journal Issue: 17; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Research Org:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org:
USDOE Office of Science (SC); Chinese Academy of Sciences (CAS)
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 60 APPLIED LIFE SCIENCES
OSTI Identifier:
1378739