Methionine Availability in the Arthropod Intestine Is Elucidated through Identification of Vibrio cholerae Methionine Acquisition Systems

While only a subset of strains are human diarrheal pathogens, all are aquatic organisms. In this environment, they often persist in close association with arthropods. In the intestinal lumen of the model arthropod , methionine and methionine sulfoxide decrease susceptibility to infection. In additio...

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Bibliographic Details
Published in:Applied and environmental microbiology 2020-05, Vol.86 (11)
Main Authors: Vanhove, Audrey S, Jugder, Bat-Erdene, Barraza, Daniela, Watnick, Paula I
Format: Article
Language:English
Subjects:
Affinity
Aquatic environment
Aquatic organisms
Arthropods
Bacteria
Colonization
Diarrhea
Drosophila
Genetics and Molecular Biology
Genomes
Insects
Intestine
Life Sciences
Methionine
Methylation
Microbiology and Parasitology
Oxidation
Proteins
Reductase
Reductases
Reduction
Sulfoxides
Vibrio cholerae
Waterborne diseases
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Summary:While only a subset of strains are human diarrheal pathogens, all are aquatic organisms. In this environment, they often persist in close association with arthropods. In the intestinal lumen of the model arthropod , methionine and methionine sulfoxide decrease susceptibility to infection. In addition to its structural role in proteins, methionine participates in the methionine cycle, which carries out synthetic and regulatory methylation reactions. It is, therefore, essential for the growth of both animals and bacteria. Methionine is scarce in some environments, and the facile conversion of free methionine to methionine sulfoxide in oxidizing environments interferes with its utilization. To ensure an adequate supply of methionine, the genomes of most organisms encode multiple high-affinity uptake pathways for methionine as well as multiple methionine sulfoxide reductases, which reduce free and protein-associated methionine sulfoxide to methionine. To explore the role of methionine uptake and reduction in colonization of the arthropod intestine, we mutagenized the two high-affinity methionine transporters and five methionine sulfoxide reductases encoded in the genome. We show that MsrC is the sole methionine sulfoxide reductase active on free methionine sulfoxide. Furthermore, in the absence of methionine synthesis, high-affinity methionine uptake but not reduction is essential for colonization of the intestine. These findings allow us to place a lower limit of 0.05 mM and an upper limit of 0.5 mM on the methionine concentration in the intestine. Methionine is an essential amino acid involved in both biosynthetic and regulatory processes in the bacterial cell. To ensure an adequate supply of methionine, bacteria have evolved multiple systems to synthesize, import, and recover this amino acid. To explore the importance of methionine synthesis, transport, and recovery in any environment, all of these systems must be identified and mutagenized. Here, we have mutagenized every high-affinity methionine uptake system and methionine sulfoxide reductase encoded in the genome of the diarrheal pathogen We use this information to determine that high-affinity methionine uptake systems are sufficient to acquire methionine in the intestine of the model arthropod but are not involved in virulence and that the intestinal concentration of methionine must be between 0.05 mM and 0.5 mM.
ISSN:0099-2240
1098-5336
DOI:10.1128/AEM.00371-20