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Manganese modulates metabolic activity and redox homeostasis in translationally-blocked Lactococcus cremoris, impacting metabolic persistence, cell-culturability, and flavor formation

Avis Dwi Wahyu Nugroho, Berdien van Olst, Stephanie Agnes Bachtiar, Sjef Boeren, View ORCID ProfileMichiel Kleerebezem, View ORCID ProfileHerwig Bachmann
doi: https://doi.org/10.1101/2021.12.14.472734
Avis Dwi Wahyu Nugroho
1TiFN, 9A, 6709 PA Wageningen, The Netherlands
2Health department, NIZO Food Research, Kernhemseweg 2, 6718 ZB Ede, The Netherlands
3Host-Microbe Interactomics Group, Wageningen University & Research, De Elst 1, 6708 WD Wageningen, The Netherlands
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Berdien van Olst
1TiFN, 9A, 6709 PA Wageningen, The Netherlands
3Host-Microbe Interactomics Group, Wageningen University & Research, De Elst 1, 6708 WD Wageningen, The Netherlands
4Laboratory of Biochemistry, Stippeneng 4, 6708 WE, Wageningen University & Research, The Netherlands
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Stephanie Agnes Bachtiar
1TiFN, 9A, 6709 PA Wageningen, The Netherlands
2Health department, NIZO Food Research, Kernhemseweg 2, 6718 ZB Ede, The Netherlands
3Host-Microbe Interactomics Group, Wageningen University & Research, De Elst 1, 6708 WD Wageningen, The Netherlands
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Sjef Boeren
1TiFN, 9A, 6709 PA Wageningen, The Netherlands
4Laboratory of Biochemistry, Stippeneng 4, 6708 WE, Wageningen University & Research, The Netherlands
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Michiel Kleerebezem
1TiFN, 9A, 6709 PA Wageningen, The Netherlands
3Host-Microbe Interactomics Group, Wageningen University & Research, De Elst 1, 6708 WD Wageningen, The Netherlands
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  • ORCID record for Michiel Kleerebezem
Herwig Bachmann
1TiFN, 9A, 6709 PA Wageningen, The Netherlands
2Health department, NIZO Food Research, Kernhemseweg 2, 6718 ZB Ede, The Netherlands
5Systems Biology Lab, Vrije Universiteit Amsterdam, De Boelelaan 1108, 1081 HZ Amsterdam, The Netherlands
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  • ORCID record for Herwig Bachmann
  • For correspondence: herwig.bachmann@nizo.com
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Abstract

Manganese (Mn) is an essential trace element that is supplemented in microbial media with varying benefits across species and growth conditions. We found that growth of Lactococcus cremoris was unaffected by manganese omission from the growth medium. The main proteome adaptation to manganese omission involved increased manganese transporter production (up to 2000-fold), while the remaining 10 significant proteome changes were between 1.4 and 4 fold. Further investigation in translationally-blocked (TB), non-growing cells showed that Mn supplementation (20 μM) led to approximately 1.5X faster acidification compared to Mn-free conditions. However, this faster acidification stagnated within 24 hours, likely due to draining of intracellular NADH that coincides with substantial loss of culturability. Conversely, without manganese, non-growing cells persisted to acidify for weeks, albeit at a reduced rate, but maintaining redox balance and culturability. Strikingly, despite being unculturable, α-keto acid-derived aldehydes continued to accumulate in cells incubated in the presence of manganese, whereas without manganese cells predominantly formed the corresponding alcohols. This is most likely reflecting NADH availability for the alcohol dehydrogenase-catalyzed conversion. Overall, manganese influences the lactococcal acidification rate, and flavor formation capacity in a redox dependent manner. These are important industrial traits especially during cheese ripening, where cells are in a non-growing, often unculturable state.

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Posted December 15, 2021.
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Manganese modulates metabolic activity and redox homeostasis in translationally-blocked Lactococcus cremoris, impacting metabolic persistence, cell-culturability, and flavor formation
Avis Dwi Wahyu Nugroho, Berdien van Olst, Stephanie Agnes Bachtiar, Sjef Boeren, Michiel Kleerebezem, Herwig Bachmann
bioRxiv 2021.12.14.472734; doi: https://doi.org/10.1101/2021.12.14.472734
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Manganese modulates metabolic activity and redox homeostasis in translationally-blocked Lactococcus cremoris, impacting metabolic persistence, cell-culturability, and flavor formation
Avis Dwi Wahyu Nugroho, Berdien van Olst, Stephanie Agnes Bachtiar, Sjef Boeren, Michiel Kleerebezem, Herwig Bachmann
bioRxiv 2021.12.14.472734; doi: https://doi.org/10.1101/2021.12.14.472734

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