Acidotolerant Bacteria and Fungi as a Sink of Methanol-Derived Carbon in a Deciduous Forest Soil

Methanol is an abundant atmospheric volatile organic compound that is released from both living and decaying plant material. In forest and other aerated soils, methanol can be consumed by methanol-utilizing microorganisms that constitute a known terrestrial sink. However, the environmental factors t...

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Main Authors: Mareen Morawe, Henrike Hoeke, Dirk K. Wissenbach, Guillaume Lentendu, Tesfaye Wubet, Eileen Kröber, Steffen Kolb
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-07-01
Series:Frontiers in Microbiology
Subjects:
pH
Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2017.01361/full
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spelling doaj-4031af7262e94107a89883aa7b103fa12020-11-24T23:50:24ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-07-01810.3389/fmicb.2017.01361267713Acidotolerant Bacteria and Fungi as a Sink of Methanol-Derived Carbon in a Deciduous Forest SoilMareen Morawe0Henrike Hoeke1Henrike Hoeke2Dirk K. Wissenbach3Guillaume Lentendu4Tesfaye Wubet5Eileen Kröber6Steffen Kolb7Steffen Kolb8Department of Ecological Microbiology, University of BayreuthBayreuth, GermanyDepartment of Molecular Systems Biology, Helmholtz Centre for Environmental ResearchLeipzig, GermanyDepartment of Pharmaceutical and Medicinal Chemistry, Institute of Pharmacy, University of LeipzigLeipzig, GermanyInstitute of Forensic Medicine, University Hospital JenaJena, GermanyDepartment of Ecology, University of KaiserslauternKaiserslautern, GermanyDepartment of Soil Ecology, Helmholtz Centre for Environmental ResearchLeipzig, GermanyInstitute of Landscape Biogeochemistry, Leibniz Centre for Landscape ResearchMüncheberg, GermanyDepartment of Ecological Microbiology, University of BayreuthBayreuth, GermanyInstitute of Landscape Biogeochemistry, Leibniz Centre for Landscape ResearchMüncheberg, GermanyMethanol is an abundant atmospheric volatile organic compound that is released from both living and decaying plant material. In forest and other aerated soils, methanol can be consumed by methanol-utilizing microorganisms that constitute a known terrestrial sink. However, the environmental factors that drive the biodiversity of such methanol-utilizers have been hardly resolved. Soil-derived isolates of methanol-utilizers can also often assimilate multicarbon compounds as alternative substrates. Here, we conducted a comparative DNA stable isotope probing experiment under methylotrophic (only [13C1]-methanol was supplemented) and combined substrate conditions ([12C1]-methanol and alternative multi-carbon [13Cu]-substrates were simultaneously supplemented) to (i) identify methanol-utilizing microorganisms of a deciduous forest soil (European beech dominated temperate forest in Germany), (ii) assess their substrate range in the soil environment, and (iii) evaluate their trophic links to other soil microorganisms. The applied multi-carbon substrates represented typical intermediates of organic matter degradation, such as acetate, plant-derived sugars (xylose and glucose), and a lignin-derived aromatic compound (vanillic acid). An experimentally induced pH shift was associated with substantial changes of the diversity of active methanol-utilizers suggesting that soil pH was a niche-defining factor of these microorganisms. The main bacterial methanol-utilizers were members of the Beijerinckiaceae (Bacteria) that played a central role in a detected methanol-based food web. A clear preference for methanol or multi-carbon substrates as carbon source of different Beijerinckiaceae-affiliated phylotypes was observed suggesting a restricted substrate range of the methylotrophic representatives. Apart from Bacteria, we also identified the yeasts Cryptococcus and Trichosporon as methanol-derived carbon-utilizing fungi suggesting that further research is needed to exclude or prove methylotrophy of these fungi.http://journal.frontiersin.org/article/10.3389/fmicb.2017.01361/fullDNA stable isotope probingmxaFbacterial 16S rRNA genefungal ITSpHhigh-throughput sequencing
collection DOAJ
language English
format Article
sources DOAJ
author Mareen Morawe
Henrike Hoeke
Henrike Hoeke
Dirk K. Wissenbach
Guillaume Lentendu
Tesfaye Wubet
Eileen Kröber
Steffen Kolb
Steffen Kolb
spellingShingle Mareen Morawe
Henrike Hoeke
Henrike Hoeke
Dirk K. Wissenbach
Guillaume Lentendu
Tesfaye Wubet
Eileen Kröber
Steffen Kolb
Steffen Kolb
Acidotolerant Bacteria and Fungi as a Sink of Methanol-Derived Carbon in a Deciduous Forest Soil
Frontiers in Microbiology
DNA stable isotope probing
mxaF
bacterial 16S rRNA gene
fungal ITS
pH
high-throughput sequencing
author_facet Mareen Morawe
Henrike Hoeke
Henrike Hoeke
Dirk K. Wissenbach
Guillaume Lentendu
Tesfaye Wubet
Eileen Kröber
Steffen Kolb
Steffen Kolb
author_sort Mareen Morawe
title Acidotolerant Bacteria and Fungi as a Sink of Methanol-Derived Carbon in a Deciduous Forest Soil
title_short Acidotolerant Bacteria and Fungi as a Sink of Methanol-Derived Carbon in a Deciduous Forest Soil
title_full Acidotolerant Bacteria and Fungi as a Sink of Methanol-Derived Carbon in a Deciduous Forest Soil
title_fullStr Acidotolerant Bacteria and Fungi as a Sink of Methanol-Derived Carbon in a Deciduous Forest Soil
title_full_unstemmed Acidotolerant Bacteria and Fungi as a Sink of Methanol-Derived Carbon in a Deciduous Forest Soil
title_sort acidotolerant bacteria and fungi as a sink of methanol-derived carbon in a deciduous forest soil
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2017-07-01
description Methanol is an abundant atmospheric volatile organic compound that is released from both living and decaying plant material. In forest and other aerated soils, methanol can be consumed by methanol-utilizing microorganisms that constitute a known terrestrial sink. However, the environmental factors that drive the biodiversity of such methanol-utilizers have been hardly resolved. Soil-derived isolates of methanol-utilizers can also often assimilate multicarbon compounds as alternative substrates. Here, we conducted a comparative DNA stable isotope probing experiment under methylotrophic (only [13C1]-methanol was supplemented) and combined substrate conditions ([12C1]-methanol and alternative multi-carbon [13Cu]-substrates were simultaneously supplemented) to (i) identify methanol-utilizing microorganisms of a deciduous forest soil (European beech dominated temperate forest in Germany), (ii) assess their substrate range in the soil environment, and (iii) evaluate their trophic links to other soil microorganisms. The applied multi-carbon substrates represented typical intermediates of organic matter degradation, such as acetate, plant-derived sugars (xylose and glucose), and a lignin-derived aromatic compound (vanillic acid). An experimentally induced pH shift was associated with substantial changes of the diversity of active methanol-utilizers suggesting that soil pH was a niche-defining factor of these microorganisms. The main bacterial methanol-utilizers were members of the Beijerinckiaceae (Bacteria) that played a central role in a detected methanol-based food web. A clear preference for methanol or multi-carbon substrates as carbon source of different Beijerinckiaceae-affiliated phylotypes was observed suggesting a restricted substrate range of the methylotrophic representatives. Apart from Bacteria, we also identified the yeasts Cryptococcus and Trichosporon as methanol-derived carbon-utilizing fungi suggesting that further research is needed to exclude or prove methylotrophy of these fungi.
topic DNA stable isotope probing
mxaF
bacterial 16S rRNA gene
fungal ITS
pH
high-throughput sequencing
url http://journal.frontiersin.org/article/10.3389/fmicb.2017.01361/full
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