Heme Uptake in Evidenced by a New Energy Coupling Factor (ECF)-Like Transport System.

Emilie Verplaetse, Gwenaëlle André-Leroux, Philippe Duhutrel, Gwendoline Coeuret, Stéphane Chaillou, Christina Nielsen-Leroux, Marie-Christine Champomier-Vergès
Author Information
  1. Emilie Verplaetse: Université Paris-Saclay, INRAE, AgroParisTech, Micalis Institute, Jouy-en-Josas, France.
  2. Gwenaëlle André-Leroux: Université Paris-Saclay, INRAE, MaIAGE, Jouy-en-Josas, France.
  3. Philippe Duhutrel: Université Paris-Saclay, INRAE, AgroParisTech, Micalis Institute, Jouy-en-Josas, France.
  4. Gwendoline Coeuret: Université Paris-Saclay, INRAE, AgroParisTech, Micalis Institute, Jouy-en-Josas, France.
  5. Stéphane Chaillou: Université Paris-Saclay, INRAE, AgroParisTech, Micalis Institute, Jouy-en-Josas, France.
  6. Christina Nielsen-Leroux: Université Paris-Saclay, INRAE, AgroParisTech, Micalis Institute, Jouy-en-Josas, France.
  7. Marie-Christine Champomier-Vergès: Université Paris-Saclay, INRAE, AgroParisTech, Micalis Institute, Jouy-en-Josas, France marie-christine.champomier-verges@inrae.fr. ORCID

Abstract

is a nonpathogenic lactic acid bacterium and a natural inhabitant of meat ecosystems. Although red meat is a heme-rich environment, does not need iron or heme for growth, although it possesses a heme-dependent catalase. Iron incorporation into from myoglobin and hemoglobin was previously shown by microscopy and the genome reveals the complete equipment for iron and heme transport. Here, we report the characterization of a five-gene cluster (from to []) encoding a putative metal iron ABC transporter. Interestingly, this cluster, together with a heme-dependent catalase gene, is also conserved in other species from the meat ecosystem. Our bioinformatic analyses revealed that the locus might correspond to a complete machinery of an energy coupling factor (ECF) transport system. We quantified the intracellular heme in the wild type (WT) and in our Δ deletion mutant using an intracellular heme sensor and inductively coupled plasma mass spectrometry for quantifying incorporated Fe heme. We showed that in the WT , heme accumulation occurs rapidly and massively in the presence of hemin, while the deletion mutant was impaired in heme uptake; this ability was restored by in complementation. Our results establish the main role of the Lsa1836-1840 ECF-like system in heme uptake. Therefore, this research outcome sheds new light on other possible functions of ECF-like systems. is a nonpathogenic bacterial species exhibiting high fitness in heme-rich environments such as meat products, although it does not need iron or heme for growth. Heme capture and utilization capacities are often associated with pathogenic species and are considered virulence-associated factors in the infected hosts. For these reasons, iron acquisition systems have been deeply studied in such species, while for nonpathogenic bacteria the information is scarce. Genomic data revealed that several putative iron transporters are present in the genome of the lactic acid bacterium In this study, we demonstrate that one of them is an ECF-like ABC transporter with a functional role in heme transport. Such evidence has not yet been brought for an ECF; therefore, our study reveals a new class of heme transport system.

Keywords

References

  1. Microb Cell Fact. 2009 May 29;8:28 [PMID: 19480672]
  2. Appl Environ Microbiol. 2005 Nov;71(11):7567-70 [PMID: 16269805]
  3. Proc Natl Acad Sci U S A. 2006 Mar 21;103(12):4386-91 [PMID: 16537422]
  4. Adv Microb Physiol. 2012;61:69-124 [PMID: 23046952]
  5. PLoS Pathog. 2010 Apr 22;6(4):e1000860 [PMID: 20421944]
  6. J Biol Chem. 2012 Mar 23;287(13):10623-10630 [PMID: 22308037]
  7. Appl Environ Microbiol. 2000 Oct;66(10):4272-8 [PMID: 11010870]
  8. Proc Natl Acad Sci U S A. 2007 Oct 30;104(44):17311-6 [PMID: 17954916]
  9. Infect Immun. 2003 Mar;71(3):1042-55 [PMID: 12595414]
  10. Appl Environ Microbiol. 1998 Apr;64(4):1359-65 [PMID: 9546173]
  11. Int J Food Microbiol. 2004 Nov 1;96(2):149-64 [PMID: 15364469]
  12. J Biol Chem. 2001 Aug 3;276(31):29515-9 [PMID: 11390404]
  13. Annu Rev Biochem. 2019 Jun 20;88:551-576 [PMID: 30485755]
  14. Curr Protoc Bioinformatics. 2016 Jun 20;54:5.6.1-5.6.37 [PMID: 27322406]
  15. Proc Natl Acad Sci U S A. 2014 Dec 30;111(52):18560-5 [PMID: 25512487]
  16. Appl Environ Microbiol. 2007 Oct;73(19):6144-9 [PMID: 17675432]
  17. Infect Immun. 2002 Aug;70(8):4494-500 [PMID: 12117961]
  18. J Biol Chem. 2013 Aug 30;288(35):25466-25476 [PMID: 23846701]
  19. Mol Microbiol. 2006 Feb;59(4):1185-98 [PMID: 16430693]
  20. Cell Res. 2017 May;27(5):675-687 [PMID: 28322252]
  21. Mol Microbiol. 2010 Nov;78(3):739-56 [PMID: 20807204]
  22. J Mol Biol. 1992 May 20;225(2):487-94 [PMID: 1593632]
  23. Nucleic Acids Res. 2005 Jul 1;33(Web Server issue):W244-8 [PMID: 15980461]
  24. Nucleic Acids Res. 2013 Jan;41(Database issue):D636-47 [PMID: 23193269]
  25. Appl Environ Microbiol. 2010 Jan;76(2):560-5 [PMID: 19933352]
  26. Proc Natl Acad Sci U S A. 2002 Feb 19;99(4):2293-8 [PMID: 11830639]
  27. PLoS One. 2017 Sep 14;12(9):e0184932 [PMID: 28910388]
  28. Nature. 2013 May 9;497(7448):272-6 [PMID: 23584587]
  29. PLoS One. 2014 Aug 25;9(8):e104794 [PMID: 25153520]
  30. Biochemistry. 2011 Jun 14;50(23):5108-19 [PMID: 21534572]
  31. Int J Food Microbiol. 1999 Dec 1;53(1):43-52 [PMID: 10598113]
  32. Meat Sci. 2014 Jul;97(3):332-8 [PMID: 24041591]
  33. Nat Biotechnol. 2005 Dec;23(12):1527-33 [PMID: 16273110]
  34. Microorganisms. 2017 Sep 06;5(3): [PMID: 28878171]
  35. Curr Opin Biotechnol. 2011 Apr;22(2):143-9 [PMID: 21211959]
  36. J Biol Chem. 2012 Feb 10;287(7):4752-8 [PMID: 22084241]
  37. J Bacteriol. 1979 Mar;137(3):1308-14 [PMID: 108244]
  38. Antonie Van Leeuwenhoek. 2002 Aug;82(1-4):263-9 [PMID: 12369192]
  39. Appl Environ Microbiol. 1996 Jun;62(6):1922-7 [PMID: 16535331]
  40. Microbiology (Reading). 1996 May;142(5):1273-1279 [PMID: 33725790]
  41. J Mol Biol. 2016 Aug 28;428(17):3408-28 [PMID: 27019298]
  42. J Bacteriol. 2009 Jan;191(1):42-51 [PMID: 18931129]
  43. J Bacteriol. 2006 Apr;188(8):2752-60 [PMID: 16585736]
  44. Nucleic Acids Res. 2019 Jan 8;47(D1):D607-D613 [PMID: 30476243]
  45. Biochim Biophys Acta. 2015 Sep;1850(9):1930-41 [PMID: 26093289]
  46. Annu Rev Biochem. 1981;50:715-31 [PMID: 6455965]
  47. J Food Prot. 2004 Sep;67(9):1977-90 [PMID: 15453593]
  48. Microbiology (Reading). 2010 Jun;156(Pt 6):1824-1835 [PMID: 20223800]
  49. Res Microbiol. 2019 Nov - Dec;170(8):358-365 [PMID: 31283960]
  50. Mol Microbiol. 2014 Aug;93(4):823-33 [PMID: 25040434]
  51. Nature. 2013 May 9;497(7448):268-71 [PMID: 23584589]
  52. J Bacteriol. 2006 Dec;188(23):8145-52 [PMID: 17012401]
  53. Biometals. 2007 Jun;20(3-4):333-45 [PMID: 17387580]
  54. Science. 2003 Feb 7;299(5608):906-9 [PMID: 12574635]
  55. Annu Rev Biochem. 2017 Jun 20;86:799-823 [PMID: 28426241]
  56. Appl Environ Microbiol. 2003 Sep;69(9):5574-84 [PMID: 12957947]
  57. Appl Environ Microbiol. 1997 Jun;63(6):2117-23 [PMID: 9172327]
  58. Infect Immun. 2010 Dec;78(12):4977-89 [PMID: 20679437]

MeSH Term

Biological Transport
Genes, Bacterial
Heme
Latilactobacillus sakei
Multigene Family

Chemicals

Heme

Word Cloud

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