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

Abstract : Lactobacillus sakei is a non-pathogenic lactic acid bacterium and a natural inhabitant of meat ecosystems. Although red meat is a heme-rich environment, L. sakei does not need iron or heme for growth, while possessing a heme-dependent catalase. Iron incorporation into L. sakei from myoglobin and hemoglobin was formerly shown by microscopy and the L. sakei genome reveals the complete equipment for iron and heme transport. Here, we report the characterization of a five-gene cluster (lsa1836-1840) 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 in vitro the intracellular heme in wild-type (WT) and in our Δlsa1836-1840 deletion mutant using an intracellular heme sensor and ICP-Mass spectrometry for quantifying incorporated 57Fe heme. We showed that in the WT L. sakei, 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 trans complementation. Our results establish the main role of the L. sakei Lsa1836-1840 ECF-like system in heme uptake. Therefore, this research outcome sheds new light on other possible functions of ECF-like systems.Importance Lactobacillus sakei is a non-pathogenic bacterial species exhibiting high fitness in heme rich environments such as meat products, although it does not need iron nor heme for growth. Heme capture and utilization capacities are often associated with pathogenic species and are considered as virulence-associated factors in the infected hosts. For these reasons, iron acquisition systems have been deeply studied in such species, while for non-pathogenic bacteria the information is scarce. Genomic data revealed that several putative iron transporters are present in the genome of the lactic acid bacterium L. sakei. 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.
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https://hal.inrae.fr/hal-02939244
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Submitted on : Tuesday, September 15, 2020 - 2:03:57 PM
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Emilie Verplaetse, Gwenaëlle André-Leroux, Philippe Duhutrel, Gwendoline Coeuret, Stéphane Chaillou, et al.. Heme Uptake in Lactobacillus sakei Evidenced by a New Energy Coupling Factor (ECF)-Like Transport System. Applied and Environmental Microbiology, American Society for Microbiology, 2020, 86 (18), pp.1-41. ⟨10.1128/AEM.02847-19⟩. ⟨hal-02939244⟩

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