Acinetobacter calcoaceticus is Well Adapted to Withstand Intestinal Stressors and Modulate the Gut Epithelium

Background: The gastrointestinal tract has been speculated to serve as a reservoir for Acinetobacter, however little is known about the ecological fitness of Acinetobacter strains in the gut. Likewise, not much is known about the ability of Acinetobacter to consume dietary, or host derived nutrients...

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Main Authors: Janiece S. Glover, Brittney D. Browning, Taylor D. Ticer, Amy C. Engevik, Melinda A. Engevik
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-05-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2022.880024/full
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author Janiece S. Glover
Brittney D. Browning
Taylor D. Ticer
Amy C. Engevik
Melinda A. Engevik
Melinda A. Engevik
author_facet Janiece S. Glover
Brittney D. Browning
Taylor D. Ticer
Amy C. Engevik
Melinda A. Engevik
Melinda A. Engevik
author_sort Janiece S. Glover
collection DOAJ
description Background: The gastrointestinal tract has been speculated to serve as a reservoir for Acinetobacter, however little is known about the ecological fitness of Acinetobacter strains in the gut. Likewise, not much is known about the ability of Acinetobacter to consume dietary, or host derived nutrients or their capacity to modulate host gene expression. Given the increasing prevalence of Acinetobacter in the clinical setting, we sought to characterize how A. calcoaceticus responds to gut-related stressors and identify potential microbe-host interactions.Materials and Methods: To accomplish these aims, we grew clinical isolates and commercially available strains of A. calcoaceticus in minimal media with different levels of pH, osmolarity, ethanol and hydrogen peroxide. Utilization of nutrients was examined using Biolog phenotypic microarrays. To examine the interactions of A. calcoaceticus with the host, inverted murine organoids where the apical membrane is exposed to bacteria, were incubated with live A. calcoaceticus, and gene expression was examined by qPCR.Results: All strains grew modestly at pH 6, 5 and 4; indicating that these strains could tolerate passage through the gastrointestinal tract. All strains had robust growth in 0.1 and 0.5 M NaCl concentrations which mirror the small intestine, but differences were observed between strains in response to 1 M NaCl. Additionally, all strains tolerated up to 5% ethanol and 0.1% hydrogen peroxide. Biolog phenotypic microarrays revealed that A. calcoaceticus strains could use a range of nutrient sources, including monosaccharides, disaccharides, polymers, glycosides, acids, and amino acids. Interestingly, the commercially available A. calcoaceticus strains and one clinical isolate stimulated the pro-inflammatory cytokines Tnf, Kc, and Mcp-1 while all strains suppressed Muc13 and Muc2.Conclusion: Collectively, these data demonstrate that A. calcoaceticus is well adapted to dealing with environmental stressors of the gastrointestinal system. This data also points to the potential for Acinetobacter to influence the gut epithelium.
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spelling doaj.art-46d4574173ce488280404ded32ffeab72022-12-22T00:29:42ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2022-05-011310.3389/fphys.2022.880024880024Acinetobacter calcoaceticus is Well Adapted to Withstand Intestinal Stressors and Modulate the Gut EpitheliumJaniece S. Glover0Brittney D. Browning1Taylor D. Ticer2Amy C. Engevik3Melinda A. Engevik4Melinda A. Engevik5Department of Regenerative Medicine and Cell Biology, Medical University of South Carolina, Charleston, SC, United StatesDepartment of Psychiatry and Behavioral Sciences, Medical University of South Carolina, Charleston, SC, United StatesDepartment of Microbiology and Immunology, Medical University of South Carolina, Charleston, SC, United StatesDepartment of Regenerative Medicine and Cell Biology, Medical University of South Carolina, Charleston, SC, United StatesDepartment of Regenerative Medicine and Cell Biology, Medical University of South Carolina, Charleston, SC, United StatesDepartment of Microbiology and Immunology, Medical University of South Carolina, Charleston, SC, United StatesBackground: The gastrointestinal tract has been speculated to serve as a reservoir for Acinetobacter, however little is known about the ecological fitness of Acinetobacter strains in the gut. Likewise, not much is known about the ability of Acinetobacter to consume dietary, or host derived nutrients or their capacity to modulate host gene expression. Given the increasing prevalence of Acinetobacter in the clinical setting, we sought to characterize how A. calcoaceticus responds to gut-related stressors and identify potential microbe-host interactions.Materials and Methods: To accomplish these aims, we grew clinical isolates and commercially available strains of A. calcoaceticus in minimal media with different levels of pH, osmolarity, ethanol and hydrogen peroxide. Utilization of nutrients was examined using Biolog phenotypic microarrays. To examine the interactions of A. calcoaceticus with the host, inverted murine organoids where the apical membrane is exposed to bacteria, were incubated with live A. calcoaceticus, and gene expression was examined by qPCR.Results: All strains grew modestly at pH 6, 5 and 4; indicating that these strains could tolerate passage through the gastrointestinal tract. All strains had robust growth in 0.1 and 0.5 M NaCl concentrations which mirror the small intestine, but differences were observed between strains in response to 1 M NaCl. Additionally, all strains tolerated up to 5% ethanol and 0.1% hydrogen peroxide. Biolog phenotypic microarrays revealed that A. calcoaceticus strains could use a range of nutrient sources, including monosaccharides, disaccharides, polymers, glycosides, acids, and amino acids. Interestingly, the commercially available A. calcoaceticus strains and one clinical isolate stimulated the pro-inflammatory cytokines Tnf, Kc, and Mcp-1 while all strains suppressed Muc13 and Muc2.Conclusion: Collectively, these data demonstrate that A. calcoaceticus is well adapted to dealing with environmental stressors of the gastrointestinal system. This data also points to the potential for Acinetobacter to influence the gut epithelium.https://www.frontiersin.org/articles/10.3389/fphys.2022.880024/fullAcinetobacterintestineorganoidAcinetobacter calcoaceticusmetabolism
spellingShingle Janiece S. Glover
Brittney D. Browning
Taylor D. Ticer
Amy C. Engevik
Melinda A. Engevik
Melinda A. Engevik
Acinetobacter calcoaceticus is Well Adapted to Withstand Intestinal Stressors and Modulate the Gut Epithelium
Frontiers in Physiology
Acinetobacter
intestine
organoid
Acinetobacter calcoaceticus
metabolism
title Acinetobacter calcoaceticus is Well Adapted to Withstand Intestinal Stressors and Modulate the Gut Epithelium
title_full Acinetobacter calcoaceticus is Well Adapted to Withstand Intestinal Stressors and Modulate the Gut Epithelium
title_fullStr Acinetobacter calcoaceticus is Well Adapted to Withstand Intestinal Stressors and Modulate the Gut Epithelium
title_full_unstemmed Acinetobacter calcoaceticus is Well Adapted to Withstand Intestinal Stressors and Modulate the Gut Epithelium
title_short Acinetobacter calcoaceticus is Well Adapted to Withstand Intestinal Stressors and Modulate the Gut Epithelium
title_sort acinetobacter calcoaceticus is well adapted to withstand intestinal stressors and modulate the gut epithelium
topic Acinetobacter
intestine
organoid
Acinetobacter calcoaceticus
metabolism
url https://www.frontiersin.org/articles/10.3389/fphys.2022.880024/full
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AT taylordticer acinetobactercalcoaceticusiswelladaptedtowithstandintestinalstressorsandmodulatethegutepithelium
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