Impact of plants on the diversity and activity of methylotrophs in soil

Abstract Background Methanol is the second most abundant volatile organic compound in the atmosphere, with the majority produced as a metabolic by-product during plant growth. There is a large disparity between the estimated amount of methanol produced by plants and the amount which escapes to the a...

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Main Authors: Michael C. Macey, Jennifer Pratscher, Andrew T. Crombie, J. Colin Murrell
Format: Article
Language:English
Published: BMC 2020-03-01
Series:Microbiome
Subjects:
Online Access:http://link.springer.com/article/10.1186/s40168-020-00801-4
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author Michael C. Macey
Jennifer Pratscher
Andrew T. Crombie
J. Colin Murrell
author_facet Michael C. Macey
Jennifer Pratscher
Andrew T. Crombie
J. Colin Murrell
author_sort Michael C. Macey
collection DOAJ
description Abstract Background Methanol is the second most abundant volatile organic compound in the atmosphere, with the majority produced as a metabolic by-product during plant growth. There is a large disparity between the estimated amount of methanol produced by plants and the amount which escapes to the atmosphere. This may be due to utilisation of methanol by plant-associated methanol-consuming bacteria (methylotrophs). The use of molecular probes has previously been effective in characterising the diversity of methylotrophs within the environment. Here, we developed and applied molecular probes in combination with stable isotope probing to identify the diversity, abundance and activity of methylotrophs in bulk and in plant-associated soils. Results Application of probes for methanol dehydrogenase genes (mxaF, xoxF, mdh2) in bulk and plant-associated soils revealed high levels of diversity of methylotrophic bacteria within the bulk soil, including Hyphomicrobium, Methylobacterium and members of the Comamonadaceae. The community of methylotrophic bacteria captured by this sequencing approach changed following plant growth. This shift in methylotrophic diversity was corroborated by identification of the active methylotrophs present in the soils by DNA stable isotope probing using 13C-labelled methanol. Sequencing of the 16S rRNA genes and construction of metagenomes from the 13C-labelled DNA revealed members of the Methylophilaceae as highly abundant and active in all soils examined. There was greater diversity of active members of the Methylophilaceae and Comamonadaceae and of the genus Methylobacterium in plant-associated soils compared to the bulk soil. Incubating growing pea plants in a 13CO2 atmosphere revealed that several genera of methylotrophs, as well as heterotrophic genera within the Actinomycetales, assimilated plant exudates in the pea rhizosphere. Conclusion In this study, we show that plant growth has a major impact on both the diversity and the activity of methanol-utilising methylotrophs in the soil environment, and thus, the study contributes significantly to efforts to balance the terrestrial methanol and carbon cycle. Video abstract
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spelling doaj.art-7ef57e5231a74440bbf375809761bcc82022-12-21T19:51:41ZengBMCMicrobiome2049-26182020-03-018111710.1186/s40168-020-00801-4Impact of plants on the diversity and activity of methylotrophs in soilMichael C. Macey0Jennifer Pratscher1Andrew T. Crombie2J. Colin Murrell3School of Environmental Sciences, University of East AngliaThe Lyell Centre, School of Energy, Geoscience, Infrastructure and Society, Heriot-Watt UniversitySchool of Biological Sciences, University of East AngliaSchool of Environmental Sciences, University of East AngliaAbstract Background Methanol is the second most abundant volatile organic compound in the atmosphere, with the majority produced as a metabolic by-product during plant growth. There is a large disparity between the estimated amount of methanol produced by plants and the amount which escapes to the atmosphere. This may be due to utilisation of methanol by plant-associated methanol-consuming bacteria (methylotrophs). The use of molecular probes has previously been effective in characterising the diversity of methylotrophs within the environment. Here, we developed and applied molecular probes in combination with stable isotope probing to identify the diversity, abundance and activity of methylotrophs in bulk and in plant-associated soils. Results Application of probes for methanol dehydrogenase genes (mxaF, xoxF, mdh2) in bulk and plant-associated soils revealed high levels of diversity of methylotrophic bacteria within the bulk soil, including Hyphomicrobium, Methylobacterium and members of the Comamonadaceae. The community of methylotrophic bacteria captured by this sequencing approach changed following plant growth. This shift in methylotrophic diversity was corroborated by identification of the active methylotrophs present in the soils by DNA stable isotope probing using 13C-labelled methanol. Sequencing of the 16S rRNA genes and construction of metagenomes from the 13C-labelled DNA revealed members of the Methylophilaceae as highly abundant and active in all soils examined. There was greater diversity of active members of the Methylophilaceae and Comamonadaceae and of the genus Methylobacterium in plant-associated soils compared to the bulk soil. Incubating growing pea plants in a 13CO2 atmosphere revealed that several genera of methylotrophs, as well as heterotrophic genera within the Actinomycetales, assimilated plant exudates in the pea rhizosphere. Conclusion In this study, we show that plant growth has a major impact on both the diversity and the activity of methanol-utilising methylotrophs in the soil environment, and thus, the study contributes significantly to efforts to balance the terrestrial methanol and carbon cycle. Video abstracthttp://link.springer.com/article/10.1186/s40168-020-00801-4MethanolRhizosphereStable isotope probingMethylotrophMethanol dehydrogenase
spellingShingle Michael C. Macey
Jennifer Pratscher
Andrew T. Crombie
J. Colin Murrell
Impact of plants on the diversity and activity of methylotrophs in soil
Microbiome
Methanol
Rhizosphere
Stable isotope probing
Methylotroph
Methanol dehydrogenase
title Impact of plants on the diversity and activity of methylotrophs in soil
title_full Impact of plants on the diversity and activity of methylotrophs in soil
title_fullStr Impact of plants on the diversity and activity of methylotrophs in soil
title_full_unstemmed Impact of plants on the diversity and activity of methylotrophs in soil
title_short Impact of plants on the diversity and activity of methylotrophs in soil
title_sort impact of plants on the diversity and activity of methylotrophs in soil
topic Methanol
Rhizosphere
Stable isotope probing
Methylotroph
Methanol dehydrogenase
url http://link.springer.com/article/10.1186/s40168-020-00801-4
work_keys_str_mv AT michaelcmacey impactofplantsonthediversityandactivityofmethylotrophsinsoil
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AT andrewtcrombie impactofplantsonthediversityandactivityofmethylotrophsinsoil
AT jcolinmurrell impactofplantsonthediversityandactivityofmethylotrophsinsoil