Metabolic pathways that permit Mycobacterium avium subsp. hominissuis to transition to different environments encountered within the host during infection

IntroductionM. avium subsp. hominissuis (M. avium) is an intracellular, facultative bacterium known to colonize and infect the human host through ingestion or respiratory inhalation. The majority of pulmonary infections occur in association with pre- existing lung diseases, such as bronchiectasis, c...

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Main Authors: Norah Abukhalid, Rajoana Rojony, Lia Danelishvili, Luiz E. Bermudez
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-04-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2023.1092317/full
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author Norah Abukhalid
Norah Abukhalid
Norah Abukhalid
Rajoana Rojony
Lia Danelishvili
Lia Danelishvili
Luiz E. Bermudez
Luiz E. Bermudez
author_facet Norah Abukhalid
Norah Abukhalid
Norah Abukhalid
Rajoana Rojony
Lia Danelishvili
Lia Danelishvili
Luiz E. Bermudez
Luiz E. Bermudez
author_sort Norah Abukhalid
collection DOAJ
description IntroductionM. avium subsp. hominissuis (M. avium) is an intracellular, facultative bacterium known to colonize and infect the human host through ingestion or respiratory inhalation. The majority of pulmonary infections occur in association with pre- existing lung diseases, such as bronchiectasis, cystic fibrosis, or chronic obstructive pulmonary disease. M. avium is also acquired by the gastrointestinal route in immunocompromised individuals such as human immunodeficiency virus HIV-1 patients leading to disseminated disease. A hallmark of M. avium pulmonary infections is the ability of pathogen to form biofilms. In addition, M. avium can reside within granulomas of low oxygen and limited nutrient conditions while establishing a persistent niche through metabolic adaptations.MethodsBacterial metabolic pathways used by M. avium within the host environment, however, are poorly understood. In this study, we analyzed M. avium proteome with a focus on core metabolic pathways expressed in the anaerobic, biofilm and aerobic conditions and that can be used by the pathogen to transition from one environment to another.ResultsOverall, 3,715 common proteins were identified between all studied conditions and proteins with increased synthesis over the of the level of expression in aerobic condition were selected for analysis of in specific metabolic pathways. The data obtained from the M. avium proteome of biofilm phenotype demonstrates in enrichment of metabolic pathways involved in the fatty acid metabolism and biosynthesis of aromatic amino acid and cofactors. Here, we also highlight the importance of chloroalkene degradation pathway and anaerobic fermentationthat enhance during the transition of M. avium from aerobic to anaerobic condition. It was also found that the production of fumarate and succinate by MAV_0927, a conserved hypothetical protein, is essential for M. avium survival and for withstanding the stress condition in biofilm. In addition, the participation of regulatory genes/proteins such as the TetR family MAV_5151 appear to be necessary for M. avium survival under biofilm and anaerobic conditions.ConclusionCollectively, our data reveal important core metabolic pathways that M. avium utilize under different stress conditions that allow the pathogen to survive in diverse host environments.
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spelling doaj.art-24223fdb2ce04e93b55b9e0c75e4cf8e2023-04-14T04:47:04ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882023-04-011310.3389/fcimb.2023.10923171092317Metabolic pathways that permit Mycobacterium avium subsp. hominissuis to transition to different environments encountered within the host during infectionNorah Abukhalid0Norah Abukhalid1Norah Abukhalid2Rajoana Rojony3Lia Danelishvili4Lia Danelishvili5Luiz E. Bermudez6Luiz E. Bermudez7Department of Biomedical Sciences, College of Veterinary Medicine, Oregon State University, Corvallis, OR, United StatesCollege of Applied Medical Sciences, King Saud bin Abdulaziz University for Health Sciences, Riyadh, Saudi ArabiaKing Abdullah International Medical Research Center, Riyadh, Saudi ArabiaDepartment of Biomedical Sciences, College of Veterinary Medicine, Oregon State University, Corvallis, OR, United StatesDepartment of Biomedical Sciences, College of Veterinary Medicine, Oregon State University, Corvallis, OR, United StatesDepartment of Microbiology, College of Science, Oregon State University, Corvallis, OR, United StatesDepartment of Biomedical Sciences, College of Veterinary Medicine, Oregon State University, Corvallis, OR, United StatesDepartment of Microbiology, College of Science, Oregon State University, Corvallis, OR, United StatesIntroductionM. avium subsp. hominissuis (M. avium) is an intracellular, facultative bacterium known to colonize and infect the human host through ingestion or respiratory inhalation. The majority of pulmonary infections occur in association with pre- existing lung diseases, such as bronchiectasis, cystic fibrosis, or chronic obstructive pulmonary disease. M. avium is also acquired by the gastrointestinal route in immunocompromised individuals such as human immunodeficiency virus HIV-1 patients leading to disseminated disease. A hallmark of M. avium pulmonary infections is the ability of pathogen to form biofilms. In addition, M. avium can reside within granulomas of low oxygen and limited nutrient conditions while establishing a persistent niche through metabolic adaptations.MethodsBacterial metabolic pathways used by M. avium within the host environment, however, are poorly understood. In this study, we analyzed M. avium proteome with a focus on core metabolic pathways expressed in the anaerobic, biofilm and aerobic conditions and that can be used by the pathogen to transition from one environment to another.ResultsOverall, 3,715 common proteins were identified between all studied conditions and proteins with increased synthesis over the of the level of expression in aerobic condition were selected for analysis of in specific metabolic pathways. The data obtained from the M. avium proteome of biofilm phenotype demonstrates in enrichment of metabolic pathways involved in the fatty acid metabolism and biosynthesis of aromatic amino acid and cofactors. Here, we also highlight the importance of chloroalkene degradation pathway and anaerobic fermentationthat enhance during the transition of M. avium from aerobic to anaerobic condition. It was also found that the production of fumarate and succinate by MAV_0927, a conserved hypothetical protein, is essential for M. avium survival and for withstanding the stress condition in biofilm. In addition, the participation of regulatory genes/proteins such as the TetR family MAV_5151 appear to be necessary for M. avium survival under biofilm and anaerobic conditions.ConclusionCollectively, our data reveal important core metabolic pathways that M. avium utilize under different stress conditions that allow the pathogen to survive in diverse host environments.https://www.frontiersin.org/articles/10.3389/fcimb.2023.1092317/fullM. aviumproteomicsaerobicanaerobicbiofilmstress conditions
spellingShingle Norah Abukhalid
Norah Abukhalid
Norah Abukhalid
Rajoana Rojony
Lia Danelishvili
Lia Danelishvili
Luiz E. Bermudez
Luiz E. Bermudez
Metabolic pathways that permit Mycobacterium avium subsp. hominissuis to transition to different environments encountered within the host during infection
Frontiers in Cellular and Infection Microbiology
M. avium
proteomics
aerobic
anaerobic
biofilm
stress conditions
title Metabolic pathways that permit Mycobacterium avium subsp. hominissuis to transition to different environments encountered within the host during infection
title_full Metabolic pathways that permit Mycobacterium avium subsp. hominissuis to transition to different environments encountered within the host during infection
title_fullStr Metabolic pathways that permit Mycobacterium avium subsp. hominissuis to transition to different environments encountered within the host during infection
title_full_unstemmed Metabolic pathways that permit Mycobacterium avium subsp. hominissuis to transition to different environments encountered within the host during infection
title_short Metabolic pathways that permit Mycobacterium avium subsp. hominissuis to transition to different environments encountered within the host during infection
title_sort metabolic pathways that permit mycobacterium avium subsp hominissuis to transition to different environments encountered within the host during infection
topic M. avium
proteomics
aerobic
anaerobic
biofilm
stress conditions
url https://www.frontiersin.org/articles/10.3389/fcimb.2023.1092317/full
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