Elsevier

Pedosphere

Volume 30, Issue 1, February 2020, Pages 62-72
Pedosphere

Long-term submergence of non-methanogenic oxic upland field soils helps to develop the methanogenic archaeal community as revealed by pot and field experiments

https://doi.org/10.1016/S1002-0160(19)60819-2Get rights and content

Abstract

The community structure of methanogenic archaea is relatively stable, i.e., it is sustained at a high abundance with minimal changes in composition, in paddy field soils irrespective of submergence and drainage. In contrast, the abundance in non-methanogenic oxic soils is much lower than that in paddy field soils. This study aimed to describe methanogenic archaeal community development following the long-term submergence of non-methanogenic oxic upland field soils in pot and field experiments. In the pot experiment, a soil sample obtained from an upland field was incubated under submerged conditions for 275 d. Soil samples periodically collected were subjected to culture-dependent most probable number (MPN) enumeration, polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE) analysis of archaeal 16S rRNA gene, and quantitative PCR analysis of the methyl-coenzyme M reductase alpha subunit gene (mcrA) of methanogenic archaea. The abundance of methanogenic archaea increased from 102 to 103 cells g−1 dry soil and 104 to 107 copies of mcrA gene g−1 dry soil after submergence. Although no methanogenic archaeon was detected prior to incubation by the DGGE analysis, members from Methanocellales, Methanosarcinaceae, and Methanosaetaceae proliferated in the soils, and the community structure was relatively stable once established. In the field experiment, the number of viable methanogenic archaea in a rice paddy field converted from meadow (reclaimed paddy field) was monitored by MPN enumeration over five annual cycles of field operations. Viability was also determined simultaneously in a paddy field where the plow layer soil from a farmer's paddy field was dressed onto the meadow (dressed paddy field) and an upland crop field converted from the meadow (reclaimed upland field). The number of viable methanogenic archaea in the reclaimed paddy field was below the detection limit before the first cultivation of rice and in the reclaimed upland field. Then, the number gradually increased over five years and finally reached 103–104 cells g−1 dry soil, which was comparable to that in the dressed paddy field. These findings showed that the low abundance of autochthonous methanogenic archaea in the non-methanogenic oxic upland field soils steadily proliferated, and the community structure was developed following repeated and long-term submergence. These results suggest that habitats suitable for methanogenic archaea were established in soil following repeated and long-term submergence.

REFERENCES (51)

  • T Watanabe et al.

    DGGE method for analyzing 16S rDNA of methanogenic archaeal community in paddy field soil

    FEMS Microbiol Lett

    (2004)
  • T Watanabe et al.

    Changes in community structure of methanogenic archaea brought about by water-saving practice in paddy field soil

    Soil Biol Biochem

    (2013)
  • T Watanabe et al.

    Community structure of methanogenic archaea in paddy field soil under double cropping (rice-wheat)

    Soil Biol Biochem

    (2006)
  • T Watanabe et al.

    Dynamics of methanogenic archaeal communities based on rRNA analysis and their relation to methanogenic activity in Japanese paddy field soils

    Soil Biol Biochem

    (2007)
  • T Watanabe et al.

    Assimilation of glucose-derived carbon into methanogenic archaea in soil under unflooded condition

    Appl Soil Ecol

    (2011)
  • R Angel et al.

    Activation of methanogenesis in arid biological soil crusts despite the presence of oxygen

    PLoS ONE

    (2011)
  • R Angel et al.

    Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions

    ISME J

    (2012)
  • S Aoki

    Black-box (in Japanese)

  • S Asakawa et al.

    Characterization of Methanosarcina mazeii TMA isolated from a paddy field soil

    Curr Microbiol

    (1995)
  • S Asakawa et al.

    Populations of methanogenic bacteria in paddy field soil under double cropping conditions (rice-wheat)

    Biol Fertil Soils

    (1995)
  • S Asakawa et al.

    Characterization of Methanobrevibacter arboriphilicus SA isolated from a paddy field soil and DNA-DNA hybridization among M. arboriphilicus strains

    Int J Syst Bacteriol

    (1993)
  • B Breidenbach et al.

    Crop rotation of flooded rice with upland maize impacts the resident and active methanogenic microbial community

    Environ Microbiol

    (2016)
  • B Breidenbach et al.

    Seasonal dynamics of bacterial and archaeal methanogenic communities in flooded rice fields and effect of drainage

    Front Microbiol

    (2015)
  • A L Brioukhanov et al.

    Aerotolerance of strictly anaerobic microorganisms and factors of defense against oxidative stress: A review

    Appl Biochem Microbiol

    (2007)
  • A L Brioukhanov et al.

    The catalase and superoxide dismutase genes are transcriptionally up-regulated upon oxidative stress in the strictly anaerobic archaeon Methanosarcina barkeri

    Microbiology

    (2006)
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    Present address: Nishi-oi, Tsukuba 300-1260, Japan.

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