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

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...

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Veröffentlicht in:Applied and environmental microbiology 2020-10, Vol.86 (21)
Hauptverfasser: 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.
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container_issue 21
container_start_page
container_title Applied and environmental microbiology
container_volume 86
creator 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.
description 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. 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
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Elaine ; Brown, Leeza ; Dawrs, Stephanie N. ; Crooks, James L. ; Chan, Edward D. ; Strong, Michael ; Nelson, Stephen T. ; Honda, Jennifer R.</creator><contributor>Alexandre, Gladys</contributor><creatorcontrib>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. ; Alexandre, Gladys</creatorcontrib><description>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. 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.</description><identifier>ISSN: 0099-2240</identifier><identifier>EISSN: 1098-5336</identifier><identifier>DOI: 10.1128/AEM.00121-20</identifier><identifier>PMID: 32859599</identifier><language>eng</language><publisher>Washington: American Society for Microbiology</publisher><subject>Aluminum ; Aluminum hydroxide ; Bayer process ; Bronchopulmonary infection ; Clay ; Disease hot spots ; Food sources ; Gibbsite ; Hematite ; Iron oxides ; Learning algorithms ; Machine learning ; Manganese ; Microbiomes ; Minerals ; Niches ; Public and Environmental Health Microbiology ; Soil chemistry ; Soil pH ; Soils</subject><ispartof>Applied and environmental microbiology, 2020-10, Vol.86 (21)</ispartof><rights>Copyright American Society for Microbiology Nov 2020</rights><rights>Copyright © 2020 Glickman et al. 2020 Glickman et al.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c389t-daa1fa9e9b1fc8feb9d35c29ef5d8148b6d0d61fac123a29c5947848fb64b0ed3</citedby><cites>FETCH-LOGICAL-c389t-daa1fa9e9b1fc8feb9d35c29ef5d8148b6d0d61fac123a29c5947848fb64b0ed3</cites><orcidid>0000-0002-4943-8738</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7580544/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7580544/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,3188,27924,27925,53791,53793</link.rule.ids></links><search><contributor>Alexandre, Gladys</contributor><creatorcontrib>Glickman, Cody M.</creatorcontrib><creatorcontrib>Virdi, Ravleen</creatorcontrib><creatorcontrib>Hasan, Nabeeh A.</creatorcontrib><creatorcontrib>Epperson, L. Elaine</creatorcontrib><creatorcontrib>Brown, Leeza</creatorcontrib><creatorcontrib>Dawrs, Stephanie N.</creatorcontrib><creatorcontrib>Crooks, James L.</creatorcontrib><creatorcontrib>Chan, Edward D.</creatorcontrib><creatorcontrib>Strong, Michael</creatorcontrib><creatorcontrib>Nelson, Stephen T.</creatorcontrib><creatorcontrib>Honda, Jennifer R.</creatorcontrib><title>Assessment of Soil Features on the Growth of Environmental Nontuberculous Mycobacterial Isolates from Hawai'i</title><title>Applied and environmental microbiology</title><description>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. 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.</description><subject>Aluminum</subject><subject>Aluminum hydroxide</subject><subject>Bayer process</subject><subject>Bronchopulmonary infection</subject><subject>Clay</subject><subject>Disease hot spots</subject><subject>Food sources</subject><subject>Gibbsite</subject><subject>Hematite</subject><subject>Iron oxides</subject><subject>Learning algorithms</subject><subject>Machine learning</subject><subject>Manganese</subject><subject>Microbiomes</subject><subject>Minerals</subject><subject>Niches</subject><subject>Public and Environmental Health Microbiology</subject><subject>Soil chemistry</subject><subject>Soil pH</subject><subject>Soils</subject><issn>0099-2240</issn><issn>1098-5336</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNpVkUtLxDAUhYMoOj52_oCACzdWbx6tyUYYhlEHRl2o65CkiVNpG03SEf-9HRXB1V2cj-8eOAgdEzgnhIqL6fzuHIBQUlDYQhMCUhQlY9U2mgBIWVDKYQ_tp_QKABwqsYv2GBWlLKWcoG6akkupc33GwePH0LT42uk8RJdw6HFeOXwTw0debeJ5v25i6De0bvF96PNgXLRDG4aE7z5tMNpmF5sxXKTQ6jxKfAwdvtUfujltDtGO121yR7_3AD1fz59mt8Xy4WYxmy4Ly4TMRa018Vo6aYi3wjsja1ZaKp0va0G4MFUNdTUillCmqbSl5JeCC28qbsDV7ABd_XjfBtO52o59o27VW2w6HT9V0I36n_TNSr2EtbosBZScj4KTX0EM74NLWb2GIfZjZ0V5BQQqYBvq7IeyMaQUnf_7QEBtxlHjOOp7HEWBfQEr4IN7</recordid><startdate>20201015</startdate><enddate>20201015</enddate><creator>Glickman, Cody M.</creator><creator>Virdi, Ravleen</creator><creator>Hasan, Nabeeh A.</creator><creator>Epperson, L. 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Elaine</au><au>Brown, Leeza</au><au>Dawrs, Stephanie N.</au><au>Crooks, James L.</au><au>Chan, Edward D.</au><au>Strong, Michael</au><au>Nelson, Stephen T.</au><au>Honda, Jennifer R.</au><au>Alexandre, Gladys</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Assessment of Soil Features on the Growth of Environmental Nontuberculous Mycobacterial Isolates from Hawai'i</atitle><jtitle>Applied and environmental microbiology</jtitle><date>2020-10-15</date><risdate>2020</risdate><volume>86</volume><issue>21</issue><issn>0099-2240</issn><eissn>1098-5336</eissn><abstract>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. 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 . 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subjects Aluminum
Aluminum hydroxide
Bayer process
Bronchopulmonary infection
Clay
Disease hot spots
Food sources
Gibbsite
Hematite
Iron oxides
Learning algorithms
Machine learning
Manganese
Microbiomes
Minerals
Niches
Public and Environmental Health Microbiology
Soil chemistry
Soil pH
Soils
title Assessment of Soil Features on the Growth of Environmental Nontuberculous Mycobacterial Isolates from Hawai'i
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