Coproporphyrin III Produced by the Bacterium Glutamicibacter arilaitensis Binds Zinc and Is Upregulated by Fungi in Cheese Rinds

Bacterium-fungus interactions play key roles in the assembly of cheese rind microbial communities, but the molecular mechanisms underlying these interactions are poorly characterized. Moreover, millions of people around the world enjoy eating cheeses and cheese rinds, but our understanding of the di...

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Main Authors: Jessica L. Cleary, Shilpa Kolachina, Benjamin E. Wolfe, Laura M. Sanchez
Format: Article
Language:English
Published: American Society for Microbiology 2018-08-01
Series:mSystems
Subjects:
Online Access:https://doi.org/10.1128/mSystems.00036-18
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spelling doaj-5a78795a60b74b20bbd07c19f7da0b7b2020-11-25T01:22:04ZengAmerican Society for MicrobiologymSystems2379-50772018-08-0134e00036-1810.1128/mSystems.00036-18Coproporphyrin III Produced by the Bacterium Glutamicibacter arilaitensis Binds Zinc and Is Upregulated by Fungi in Cheese RindsJessica L. ClearyShilpa KolachinaBenjamin E. WolfeLaura M. SanchezBacterium-fungus interactions play key roles in the assembly of cheese rind microbial communities, but the molecular mechanisms underlying these interactions are poorly characterized. Moreover, millions of people around the world enjoy eating cheeses and cheese rinds, but our understanding of the diversity of microbial metabolites ingested during cheese consumption is limited. The discovery of zinc coproporphyrin III as the cause of pink pigment production by Glutamicibacter arilaitensis suggests that secretion of this molecule is important for microbial acquisition of trace metals.Microbial communities of fermented food microbiomes typically exhibit predictable patterns of microbial succession. However, the biochemical mechanisms that control the diversity and dynamics of these communities are not well described. Interactions between bacteria and fungi may be one mechanism controlling the development of cheese rind microbiomes. This study characterizes a specific bacterium-fungus interaction previously discovered on cheese rinds between the bacterium Glutamicibacter arilaitensis (formerly Arthrobacter arilaitensis) and fungi of the genus Penicillium and identifies the specialized metabolites produced during cocultures. G. arilaitensis was previously shown to produce an unknown pink pigment in response to the presence of Penicillium. Using a combination of mass spectrometry, nuclear magnetic resonance (NMR), and transcriptome sequencing (RNA-seq), we determined that this pigment production is associated with production of coproporphyrin III. The discovery that coproporphyrin III preferentially bound zinc over other trace metals found in cheese curds highlights the value of using analytical chemistry to confirm identity of predicted chemical species.https://doi.org/10.1128/mSystems.00036-18Glutamicibacter arilaitensisimaging mass spectrometrynatural rind cheesePenicilliumspecialized metaboliteszinc coproporphyrin III
collection DOAJ
language English
format Article
sources DOAJ
author Jessica L. Cleary
Shilpa Kolachina
Benjamin E. Wolfe
Laura M. Sanchez
spellingShingle Jessica L. Cleary
Shilpa Kolachina
Benjamin E. Wolfe
Laura M. Sanchez
Coproporphyrin III Produced by the Bacterium Glutamicibacter arilaitensis Binds Zinc and Is Upregulated by Fungi in Cheese Rinds
mSystems
Glutamicibacter arilaitensis
imaging mass spectrometry
natural rind cheese
Penicillium
specialized metabolites
zinc coproporphyrin III
author_facet Jessica L. Cleary
Shilpa Kolachina
Benjamin E. Wolfe
Laura M. Sanchez
author_sort Jessica L. Cleary
title Coproporphyrin III Produced by the Bacterium Glutamicibacter arilaitensis Binds Zinc and Is Upregulated by Fungi in Cheese Rinds
title_short Coproporphyrin III Produced by the Bacterium Glutamicibacter arilaitensis Binds Zinc and Is Upregulated by Fungi in Cheese Rinds
title_full Coproporphyrin III Produced by the Bacterium Glutamicibacter arilaitensis Binds Zinc and Is Upregulated by Fungi in Cheese Rinds
title_fullStr Coproporphyrin III Produced by the Bacterium Glutamicibacter arilaitensis Binds Zinc and Is Upregulated by Fungi in Cheese Rinds
title_full_unstemmed Coproporphyrin III Produced by the Bacterium Glutamicibacter arilaitensis Binds Zinc and Is Upregulated by Fungi in Cheese Rinds
title_sort coproporphyrin iii produced by the bacterium glutamicibacter arilaitensis binds zinc and is upregulated by fungi in cheese rinds
publisher American Society for Microbiology
series mSystems
issn 2379-5077
publishDate 2018-08-01
description Bacterium-fungus interactions play key roles in the assembly of cheese rind microbial communities, but the molecular mechanisms underlying these interactions are poorly characterized. Moreover, millions of people around the world enjoy eating cheeses and cheese rinds, but our understanding of the diversity of microbial metabolites ingested during cheese consumption is limited. The discovery of zinc coproporphyrin III as the cause of pink pigment production by Glutamicibacter arilaitensis suggests that secretion of this molecule is important for microbial acquisition of trace metals.Microbial communities of fermented food microbiomes typically exhibit predictable patterns of microbial succession. However, the biochemical mechanisms that control the diversity and dynamics of these communities are not well described. Interactions between bacteria and fungi may be one mechanism controlling the development of cheese rind microbiomes. This study characterizes a specific bacterium-fungus interaction previously discovered on cheese rinds between the bacterium Glutamicibacter arilaitensis (formerly Arthrobacter arilaitensis) and fungi of the genus Penicillium and identifies the specialized metabolites produced during cocultures. G. arilaitensis was previously shown to produce an unknown pink pigment in response to the presence of Penicillium. Using a combination of mass spectrometry, nuclear magnetic resonance (NMR), and transcriptome sequencing (RNA-seq), we determined that this pigment production is associated with production of coproporphyrin III. The discovery that coproporphyrin III preferentially bound zinc over other trace metals found in cheese curds highlights the value of using analytical chemistry to confirm identity of predicted chemical species.
topic Glutamicibacter arilaitensis
imaging mass spectrometry
natural rind cheese
Penicillium
specialized metabolites
zinc coproporphyrin III
url https://doi.org/10.1128/mSystems.00036-18
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