The sulfur formation system mediating extracellular cysteine-cystine recycling in Fervidobacterium islandicum AW-1 is associated with keratin degradation

Hyeon Su Jin, Immanuel Dhanasingh, Jae Yoon Sung, Jae Won La, Yena Lee, Eun Mi Lee, Yujin Kang, Do Yup Lee, Sung Haeng Lee, Dong Woo Lee

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1 Citation (Scopus)

Abstract

Most extremophilic anaerobes possess a sulfur formation (Suf) system for Fe–S cluster biogenesis. In addition to its essential role in redox chemistry and stress responses of Fe–S cluster proteins, the Suf system may play an important role in keratin degradation by Fervidobacterium islandicum AW-1. Comparative genomics of the order Thermotogales revealed that the feather-degrading F. islandicum AW-1 has a complete Suf-like machinery (SufCBDSU) that is highly expressed in cells grown on native feathers in the absence of elemental sulfur (S0). On the other hand, F. islandicum AW-1 exhibited a significant retardation in the Suf system-mediated keratin degradation in the presence of S0. Detailed differential expression analysis of sulfur assimilation machineries unveiled the mechanism by which an efficient sulfur delivery from persulfurated SufS to SufU is achieved during keratinolysis under sulfur starvation. Indeed, addition of SufS–SufU to cell extracts containing keratinolytic proteases accelerated keratin decomposition in vitro under reducing conditions. Remarkably, mass spectrometric analysis of extracellular and intracellular levels of amino acids suggested that redox homeostasis within cells coupled to extracellular cysteine and cystine recycling might be a prerequisite for keratinolysis. Taken together, these results suggest that the Suf-like machinery including the SufS–SufU complex may contribute to sulfur availability for an extracellular reducing environment as well as intracellular redox homeostasis through cysteine released from keratin hydrolysate under starvation conditions.

Original languageEnglish
Pages (from-to)938-952
Number of pages15
JournalMicrobial Biotechnology
Volume14
Issue number3
DOIs
Publication statusPublished - 2021 May

Bibliographical note

Funding Information:
This work was supported by the National Research Foundation of Korea (2017M3A9F3043837 to D.W.L. and 2016R1D1A1B03932717 to S.H.L.) funded by the Ministry of Science, ICT, and Future Planning, by the Strategic Initiative for Microbiomes in Agriculture and Food funded by the Ministry of Agriculture, Food, and Rural Affairs (918012‐4 to D.W.L.), Brain Korea 21(BK21) program (H.S.J and J.Y.S. were fellowship awardees by BK21 program), by the Korea Health Technology R&D project (HP20C0082 to D.W.L.) funded by the Ministry of Health & Welfare, and by the Yonsei University Research Fund of ICB192021 (2019‐22‐0040).

Publisher Copyright:
© 2020 The Authors. Microbial Biotechnology published by Society for Applied Microbiology and John Wiley & Sons Ltd.

All Science Journal Classification (ASJC) codes

  • Biotechnology
  • Bioengineering
  • Biochemistry
  • Applied Microbiology and Biotechnology

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