The hierarchy of sugar catabolization in Lactococcus cremoris

Bacteria adapt to nutrient availability by regulating the synthesis of enzymes. Transcriptome- and multi-sugar growth studies suggest that Lactococcus cremoris represses genes involved in the catabolization of lower growth rate-supporting (lower quality) sugars in a hierarchical order. Furthermore, L. cremoris appears to always express genes involved in the catabolization of higher growth rate-supporting sugars (higher quality) relative to the sugar it is growing on. Here, we unraveled the sugar catabolization hierarchy by determining the sugar catabolizing capacity and the proteome of cells exponentially growing on glucose (µmax = 0.72 h−1), lactose (µmax = 0.6 h−1), galactose (µmax = 0.44 h−1), or maltose (µmax = 0.43 h−1). We found that L. cremoris can grow on 14 of the 96 sugars in a Biolog plate, with µmax ranging from 0.32 to 0.72 h−1. Proteome and catabolization rate measurements show that L. cremoris consistently prepares for the catabolization of higher-quality sugars, except trehalose. While cells were not prepared for the catabolization of most lower-quality sugars, some proteins related to fructose and lactose consumption were always present. Moreover, reducing the growth rate of glucose through salt stress had only a minor influence on the sugars that L. cremoris could catabolize. These findings demonstrate that the catabolization hierarchy is not strictly linked to absolute growth rate or sugar quality. Cells instantly catabolizing a higher-quality sugar require enhanced expression of ribosomal and nucleotide metabolism functions for growth rate maximization, whereas transitioning to lower-quality sugars requires enhanced synthesis of proteins related to arginine catabolism and mixed acid fermentation, besides sugar-specific catabolic proteins.

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Main Authors: Douwenga, Sieze, van Olst, B., Boeren, J.A., Luo, Y., Lai, Xin, Teusink, Bas, Vervoort, J.J.M., Kleerebezem, M., Bachmann, H.
Format: Article/Letter to editor biblioteca
Language:English
Subjects:Life Science,
Online Access:https://research.wur.nl/en/publications/the-hierarchy-of-sugar-catabolization-in-lactococcus-cremoris
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spelling dig-wur-nl-wurpubs-6216732024-12-04 Douwenga, Sieze van Olst, B. Boeren, J.A. Luo, Y. Lai, Xin Teusink, Bas Vervoort, J.J.M. Kleerebezem, M. Bachmann, H. Article/Letter to editor Microbiology Spectrum 11 (2023) 6 ISSN: 2165-0497 The hierarchy of sugar catabolization in Lactococcus cremoris 2023 Bacteria adapt to nutrient availability by regulating the synthesis of enzymes. Transcriptome- and multi-sugar growth studies suggest that Lactococcus cremoris represses genes involved in the catabolization of lower growth rate-supporting (lower quality) sugars in a hierarchical order. Furthermore, L. cremoris appears to always express genes involved in the catabolization of higher growth rate-supporting sugars (higher quality) relative to the sugar it is growing on. Here, we unraveled the sugar catabolization hierarchy by determining the sugar catabolizing capacity and the proteome of cells exponentially growing on glucose (µmax = 0.72 h−1), lactose (µmax = 0.6 h−1), galactose (µmax = 0.44 h−1), or maltose (µmax = 0.43 h−1). We found that L. cremoris can grow on 14 of the 96 sugars in a Biolog plate, with µmax ranging from 0.32 to 0.72 h−1. Proteome and catabolization rate measurements show that L. cremoris consistently prepares for the catabolization of higher-quality sugars, except trehalose. While cells were not prepared for the catabolization of most lower-quality sugars, some proteins related to fructose and lactose consumption were always present. Moreover, reducing the growth rate of glucose through salt stress had only a minor influence on the sugars that L. cremoris could catabolize. These findings demonstrate that the catabolization hierarchy is not strictly linked to absolute growth rate or sugar quality. Cells instantly catabolizing a higher-quality sugar require enhanced expression of ribosomal and nucleotide metabolism functions for growth rate maximization, whereas transitioning to lower-quality sugars requires enhanced synthesis of proteins related to arginine catabolism and mixed acid fermentation, besides sugar-specific catabolic proteins. en application/pdf https://research.wur.nl/en/publications/the-hierarchy-of-sugar-catabolization-in-lactococcus-cremoris 10.1128/spectrum.02248-23 https://edepot.wur.nl/642607 Life Science https://creativecommons.org/licenses/by/4.0/ https://creativecommons.org/licenses/by/4.0/ Wageningen University & Research
institution WUR NL
collection DSpace
country Países bajos
countrycode NL
component Bibliográfico
access En linea
databasecode dig-wur-nl
tag biblioteca
region Europa del Oeste
libraryname WUR Library Netherlands
language English
topic Life Science
Life Science
spellingShingle Life Science
Life Science
Douwenga, Sieze
van Olst, B.
Boeren, J.A.
Luo, Y.
Lai, Xin
Teusink, Bas
Vervoort, J.J.M.
Kleerebezem, M.
Bachmann, H.
The hierarchy of sugar catabolization in Lactococcus cremoris
description Bacteria adapt to nutrient availability by regulating the synthesis of enzymes. Transcriptome- and multi-sugar growth studies suggest that Lactococcus cremoris represses genes involved in the catabolization of lower growth rate-supporting (lower quality) sugars in a hierarchical order. Furthermore, L. cremoris appears to always express genes involved in the catabolization of higher growth rate-supporting sugars (higher quality) relative to the sugar it is growing on. Here, we unraveled the sugar catabolization hierarchy by determining the sugar catabolizing capacity and the proteome of cells exponentially growing on glucose (µmax = 0.72 h−1), lactose (µmax = 0.6 h−1), galactose (µmax = 0.44 h−1), or maltose (µmax = 0.43 h−1). We found that L. cremoris can grow on 14 of the 96 sugars in a Biolog plate, with µmax ranging from 0.32 to 0.72 h−1. Proteome and catabolization rate measurements show that L. cremoris consistently prepares for the catabolization of higher-quality sugars, except trehalose. While cells were not prepared for the catabolization of most lower-quality sugars, some proteins related to fructose and lactose consumption were always present. Moreover, reducing the growth rate of glucose through salt stress had only a minor influence on the sugars that L. cremoris could catabolize. These findings demonstrate that the catabolization hierarchy is not strictly linked to absolute growth rate or sugar quality. Cells instantly catabolizing a higher-quality sugar require enhanced expression of ribosomal and nucleotide metabolism functions for growth rate maximization, whereas transitioning to lower-quality sugars requires enhanced synthesis of proteins related to arginine catabolism and mixed acid fermentation, besides sugar-specific catabolic proteins.
format Article/Letter to editor
topic_facet Life Science
author Douwenga, Sieze
van Olst, B.
Boeren, J.A.
Luo, Y.
Lai, Xin
Teusink, Bas
Vervoort, J.J.M.
Kleerebezem, M.
Bachmann, H.
author_facet Douwenga, Sieze
van Olst, B.
Boeren, J.A.
Luo, Y.
Lai, Xin
Teusink, Bas
Vervoort, J.J.M.
Kleerebezem, M.
Bachmann, H.
author_sort Douwenga, Sieze
title The hierarchy of sugar catabolization in Lactococcus cremoris
title_short The hierarchy of sugar catabolization in Lactococcus cremoris
title_full The hierarchy of sugar catabolization in Lactococcus cremoris
title_fullStr The hierarchy of sugar catabolization in Lactococcus cremoris
title_full_unstemmed The hierarchy of sugar catabolization in Lactococcus cremoris
title_sort hierarchy of sugar catabolization in lactococcus cremoris
url https://research.wur.nl/en/publications/the-hierarchy-of-sugar-catabolization-in-lactococcus-cremoris
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