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A Systems-Wide Analysis of Proteolytic and Lipolytic Pathways Uncovers The Flavor-Forming Potential of The Gram-Positive Bacterium Macrococcus caseolyticus subsp. caseolyticus
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2020-07-07
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Mazhar S., Kilcawley K. N., Hill C., McAuliffe O. A Systems-Wide Analysis of Proteolytic and Lipolytic Pathways Uncovers The Flavor-Forming Potential of The Gram-Positive Bacterium Macrococcus caseolyticus subsp. caseolyticus. Frontiers in Microbiology. 2020, 11, 1533. doi: https://doi.org/10.3389/fmicb.2020.01533
Abstract
Macrococcus caseolyticus subsp. caseolyticus is a Gram-positive, commensal
organism documented to be present as a component of the secondary microflora in
fermented foods such as Ragusano and Fontina cheeses and Cantonese sausage. In
these products, the organism appears to play a role in ripening and the development
of the final organoleptic qualities. However, the role of this organism in flavor generation
is not well understood. Therefore, the objective of this study was to investigate the
role of M. caseolyticus subsp. caseolyticus in flavor compound formation through an
examination of enzymatic, metabolomic and genomic data. A bank of M. caseolyticus
subsp. caseolyticus strains derived from a variety of niches were examined. Enzyme
activities analyzed comprised those of the proteolytic and lipolytic cascades including
cell-envelope proteinase (CEP), peptidases, esterases, lipases, aminotransferases
and glutamate dehydrogenase (GDH). Strain to strain variation was observed, often
associated with niche. All strains, except those isolated from non-dairy sources,
demonstrated high CEP activity. Such high CEP activity associated with dairy strains
implies the importance of this characteristic in the adaptation of these strains to
a dairy-specific niche. However, limited downstream peptidolytic activity, in addition
to a limited ability to generate free amino acids (FAA) was observed across all
strains, indicating weak ability of this organism to generate amino-acid derived flavor
compounds. Interestingly, the strains with high CEP activity also demonstrated high
esterase activity and gas chromatography-mass spectrometry (GC-MS) analysis of
the volatile compounds produced when these strains were grown in lactose-free milk
demonstrated differences in the range and types of volatiles produced. In contrast
to this metabolic versatility, comparative genome analysis revealed the distribution of
components of the proteolytic and lipolytic system in these strains to be conserved.
Overall, this study demonstrates the potential of M. caseolyticus subsp. caseolyticus to generate diverse volatile flavor compounds. Additionally, the identification of the highly
active strain-specific cell wall bound caseolytic proteases deriving extensive casein
hydrolysis, serves as a promising avenue which can be potentially harnessed in the
future to produce greater and more diverse flavor compounds.