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Assessment of Soil Features on the Growth of Environmental Nontuberculous Mycobacterial Isolates from Hawai'i

Environmental nontuberculous mycobacteria (NTM), with the potential to cause opportunistic lung infections, can reside in soil. This might be particularly relevant in Hawai’i, a geographic hot spot for NTM infections and whose soil composition differs from many other areas of the world. Soil compone...

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Autores principales: Glickman, Cody M., Virdi, Ravleen, Hasan, Nabeeh A., Epperson, L. Elaine, Brown, Leeza, Dawrs, Stephanie N., Crooks, James L., Chan, Edward D., Strong, Michael, Nelson, Stephen T., Honda, Jennifer R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7580544/
https://www.ncbi.nlm.nih.gov/pubmed/32859599
http://dx.doi.org/10.1128/AEM.00121-20
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author Glickman, Cody M.
Virdi, Ravleen
Hasan, Nabeeh A.
Epperson, L. Elaine
Brown, Leeza
Dawrs, Stephanie N.
Crooks, James L.
Chan, Edward D.
Strong, Michael
Nelson, Stephen T.
Honda, Jennifer R.
author_facet Glickman, Cody M.
Virdi, Ravleen
Hasan, Nabeeh A.
Epperson, L. Elaine
Brown, Leeza
Dawrs, Stephanie N.
Crooks, James L.
Chan, Edward D.
Strong, Michael
Nelson, Stephen T.
Honda, Jennifer R.
author_sort Glickman, Cody M.
collection PubMed
description Environmental nontuberculous mycobacteria (NTM), with the potential to cause opportunistic lung infections, can reside in soil. This might be particularly relevant in Hawai’i, a geographic hot spot for NTM infections and whose soil composition differs from many other areas of the world. Soil components are likely to contribute to NTM prevalence in certain niches as food sources or attachment scaffolds, but the particular types of soils, clays, and minerals that impact NTM growth are not well-defined. Hawai’i soil and chemically weathered rock (saprolite) samples were examined to characterize the microbiome and quantify 11 mineralogical features as well as soil pH. Machine learning methods were applied to identify important soil features influencing the presence of NTM. Next, these features were directly tested in vitro by incubating synthetic clays and minerals in the presence of Mycobacteroides abscessus and Mycobacterium chimaera isolates recovered from the Hawai'i environment, and changes in bacterial growth were determined. Of the components examined, synthetic gibbsite, a mineral form of aluminum hydroxide, inhibited the growth of both M. abscessus and M. chimaera, while other minerals tested showed differential effects on each species. For example, M. abscessus (but not M. chimaera) growth was significantly higher in the presence of hematite, an iron oxide mineral. In contrast, M. chimaera (but not M. abscessus) counts were significantly reduced in the presence of birnessite, a manganese-containing mineral. These studies shed new light on the mineralogic features that promote or inhibit the presence of Hawai’i NTM in Hawai’i soil. IMPORTANCE Globally and in the United States, the prevalence of NTM pulmonary disease—a potentially life-threatening but underdiagnosed chronic illness—is prominently rising. While NTM are ubiquitous in the environment, including in soil, the specific soil components that promote or inhibit NTM growth have not been elucidated. We hypothesized that NTM culture-positive soil contains minerals that promote NTM growth in vitro. Because Hawai’i is a hot spot for NTM and a unique geographic archipelago, we examined the composition of Hawai’i soil and identified individual clay, iron, and manganese minerals associated with NTM. Next, individual components were evaluated for their ability to directly modulate NTM growth in culture. In general, gibbsite and some manganese oxides were shown to decrease NTM, whereas iron-containing minerals were associated with higher NTM counts. These data provide new information to guide future analyses of soil-associated factors impacting persistence of these soil bacteria.
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spelling pubmed-75805442020-11-06 Assessment of Soil Features on the Growth of Environmental Nontuberculous Mycobacterial Isolates from Hawai'i Glickman, Cody M. Virdi, Ravleen Hasan, Nabeeh A. Epperson, L. Elaine Brown, Leeza Dawrs, Stephanie N. Crooks, James L. Chan, Edward D. Strong, Michael Nelson, Stephen T. Honda, Jennifer R. Appl Environ Microbiol Public and Environmental Health Microbiology Environmental nontuberculous mycobacteria (NTM), with the potential to cause opportunistic lung infections, can reside in soil. This might be particularly relevant in Hawai’i, a geographic hot spot for NTM infections and whose soil composition differs from many other areas of the world. Soil components are likely to contribute to NTM prevalence in certain niches as food sources or attachment scaffolds, but the particular types of soils, clays, and minerals that impact NTM growth are not well-defined. Hawai’i soil and chemically weathered rock (saprolite) samples were examined to characterize the microbiome and quantify 11 mineralogical features as well as soil pH. Machine learning methods were applied to identify important soil features influencing the presence of NTM. Next, these features were directly tested in vitro by incubating synthetic clays and minerals in the presence of Mycobacteroides abscessus and Mycobacterium chimaera isolates recovered from the Hawai'i environment, and changes in bacterial growth were determined. Of the components examined, synthetic gibbsite, a mineral form of aluminum hydroxide, inhibited the growth of both M. abscessus and M. chimaera, while other minerals tested showed differential effects on each species. For example, M. abscessus (but not M. chimaera) growth was significantly higher in the presence of hematite, an iron oxide mineral. In contrast, M. chimaera (but not M. abscessus) counts were significantly reduced in the presence of birnessite, a manganese-containing mineral. These studies shed new light on the mineralogic features that promote or inhibit the presence of Hawai’i NTM in Hawai’i soil. IMPORTANCE Globally and in the United States, the prevalence of NTM pulmonary disease—a potentially life-threatening but underdiagnosed chronic illness—is prominently rising. While NTM are ubiquitous in the environment, including in soil, the specific soil components that promote or inhibit NTM growth have not been elucidated. We hypothesized that NTM culture-positive soil contains minerals that promote NTM growth in vitro. Because Hawai’i is a hot spot for NTM and a unique geographic archipelago, we examined the composition of Hawai’i soil and identified individual clay, iron, and manganese minerals associated with NTM. Next, individual components were evaluated for their ability to directly modulate NTM growth in culture. In general, gibbsite and some manganese oxides were shown to decrease NTM, whereas iron-containing minerals were associated with higher NTM counts. These data provide new information to guide future analyses of soil-associated factors impacting persistence of these soil bacteria. American Society for Microbiology 2020-10-15 /pmc/articles/PMC7580544/ /pubmed/32859599 http://dx.doi.org/10.1128/AEM.00121-20 Text en Copyright © 2020 Glickman et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Public and Environmental Health Microbiology
Glickman, Cody M.
Virdi, Ravleen
Hasan, Nabeeh A.
Epperson, L. Elaine
Brown, Leeza
Dawrs, Stephanie N.
Crooks, James L.
Chan, Edward D.
Strong, Michael
Nelson, Stephen T.
Honda, Jennifer R.
Assessment of Soil Features on the Growth of Environmental Nontuberculous Mycobacterial Isolates from Hawai'i
title Assessment of Soil Features on the Growth of Environmental Nontuberculous Mycobacterial Isolates from Hawai'i
title_full Assessment of Soil Features on the Growth of Environmental Nontuberculous Mycobacterial Isolates from Hawai'i
title_fullStr Assessment of Soil Features on the Growth of Environmental Nontuberculous Mycobacterial Isolates from Hawai'i
title_full_unstemmed Assessment of Soil Features on the Growth of Environmental Nontuberculous Mycobacterial Isolates from Hawai'i
title_short Assessment of Soil Features on the Growth of Environmental Nontuberculous Mycobacterial Isolates from Hawai'i
title_sort assessment of soil features on the growth of environmental nontuberculous mycobacterial isolates from hawai'i
topic Public and Environmental Health Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7580544/
https://www.ncbi.nlm.nih.gov/pubmed/32859599
http://dx.doi.org/10.1128/AEM.00121-20
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