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Microbial community structure of relict niter-beds previously used for saltpeter production.

Narihiro T, Tamaki H, Akiba A, Takasaki K, Nakano K, Kamagata Y, Hanada S, Maji T - PLoS ONE (2014)

Bottom Line: The 16S rRNA gene pyrotag analysis showed that members of the phyla Proteobacteria, Actinobacteria, Bacteroidetes, Chloroflexi, Firmicutes, Gemmatimonadetes, and Planctomycetes were major microbial constituents, and principal coordinate analysis showed that the NO3-, Cl-, K+, and Na+ contents were potential determinants of the structures of entire microbial communities in relict niter-bed soils.Nitrososphaera"-type ammonia-oxidizing archaea (AOA), respectively, predominated in relict niter-bed soils.In addition, soil pH and organic carbon content were important factors for the ecological niche of AOB and AOA in relict niter-bed soil ecosystems.

View Article: PubMed Central - PubMed

Affiliation: Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Ibaraki, Japan.

ABSTRACT
From the 16th to the 18th centuries in Japan, saltpeter was produced using a biological niter-bed process and was formed under the floor of gassho-style houses in the historic villages of Shirakawa-go and Gokayama, which are classified as United Nations Educational, Scientific and Cultural Organization (UNESCO) World Heritage Sites. The relict niter-beds are now conserved in the underfloor space of gassho-style houses, where they are isolated from destabilizing environmental factors and retain the ability to produce nitrate. However, little is known about the nitrifying microbes in such relict niter-bed ecosystems. In this study, the microbial community structures within nine relict niter-bed soils were investigated using 454 pyrotag analysis targeting the 16S rRNA gene and the bacterial and archaeal ammonia monooxygenase gene (amoA). The 16S rRNA gene pyrotag analysis showed that members of the phyla Proteobacteria, Actinobacteria, Bacteroidetes, Chloroflexi, Firmicutes, Gemmatimonadetes, and Planctomycetes were major microbial constituents, and principal coordinate analysis showed that the NO3-, Cl-, K+, and Na+ contents were potential determinants of the structures of entire microbial communities in relict niter-bed soils. The bacterial and archaeal amoA libraries indicated that members of the Nitrosospira-type ammonia-oxidizing bacteria (AOB) and "Ca. Nitrososphaera"-type ammonia-oxidizing archaea (AOA), respectively, predominated in relict niter-bed soils. In addition, soil pH and organic carbon content were important factors for the ecological niche of AOB and AOA in relict niter-bed soil ecosystems.

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Distance matrix tree of bacterial amoA gene sequences retrieved from niter-bed soils based on the maximum likelihood method.Boldface indicates the sequences obtained in this study. The Nitrosococcus amoA gene sequences (AJ298699 and AJ298701) were used as outgroups. The bar indicates 10% base substitution. Branching points supported probabilities >95%, >75%, and >50% by bootstrap analyses (based on 1,000 replicates, estimated using the maximum likelihood method) are indicated by solid circle, open circles, and open square, respectively.
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pone-0104752-g002: Distance matrix tree of bacterial amoA gene sequences retrieved from niter-bed soils based on the maximum likelihood method.Boldface indicates the sequences obtained in this study. The Nitrosococcus amoA gene sequences (AJ298699 and AJ298701) were used as outgroups. The bar indicates 10% base substitution. Branching points supported probabilities >95%, >75%, and >50% by bootstrap analyses (based on 1,000 replicates, estimated using the maximum likelihood method) are indicated by solid circle, open circles, and open square, respectively.

Mentions: The most abundant AOB belonged to the genus Nitrosospira (6 OTUs, 68.13–99.96% of the total reads in each sample), and Nitrosospira briensis-type OTU (NB_Bamo_01) predominated in all samples (except for OVA1 and OVA2, in which there were no bacterial amoA gene amplification) (Table S6). This result is in good accordance with 16S rRNA gene pyrotag analysis that found a Nitrosospira briensis-type OTU (no. 673) across the samples. An OTU (NB_Bamo_01) related to the Nitrosospira briensis strain Nsp10 (95.5% amoA gene sequence identity) was detected as a major AOB population in all niter-bed soils (Fig. 2 and Table S6). Nitrosospira briensis are enriched in and have been isolated from soil samples taken from sandy and agriculturally uncultivated areas of Europe [43]. To the best of our knowledge, only two reports have described the clear appearance of Nitrosospira briensis populations: water columns of the Chesapeake Bay [44] and soil samples of the Cascade Mountains in Oregon [45] in the U.S. Interestingly, Bollmann et al. [46] reported that under ammonia-starved conditions, the cells of Nitrosospira briensis had the ability to immediately recover ammonia oxidation activity upon exposure to ammonia-rich conditions. Although the mechanism behind this phenomenon is unclear, Nitrosospira briensis-type AOB may reserve their activity in ammonia-limited environments, such as the relict niter-bed soils. Within the genus Nitrosospira, an OTU (NB_Bamo_03) that is closely related to the Nitrosospira tenuis strain Nv-12 (96.2% sequence identity) was also detected in all bacterial amoA gene pytotag libraries; however, its ecophysiological traits (other than ammonia oxidation) remain unclear.


Microbial community structure of relict niter-beds previously used for saltpeter production.

Narihiro T, Tamaki H, Akiba A, Takasaki K, Nakano K, Kamagata Y, Hanada S, Maji T - PLoS ONE (2014)

Distance matrix tree of bacterial amoA gene sequences retrieved from niter-bed soils based on the maximum likelihood method.Boldface indicates the sequences obtained in this study. The Nitrosococcus amoA gene sequences (AJ298699 and AJ298701) were used as outgroups. The bar indicates 10% base substitution. Branching points supported probabilities >95%, >75%, and >50% by bootstrap analyses (based on 1,000 replicates, estimated using the maximum likelihood method) are indicated by solid circle, open circles, and open square, respectively.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4128746&req=5

pone-0104752-g002: Distance matrix tree of bacterial amoA gene sequences retrieved from niter-bed soils based on the maximum likelihood method.Boldface indicates the sequences obtained in this study. The Nitrosococcus amoA gene sequences (AJ298699 and AJ298701) were used as outgroups. The bar indicates 10% base substitution. Branching points supported probabilities >95%, >75%, and >50% by bootstrap analyses (based on 1,000 replicates, estimated using the maximum likelihood method) are indicated by solid circle, open circles, and open square, respectively.
Mentions: The most abundant AOB belonged to the genus Nitrosospira (6 OTUs, 68.13–99.96% of the total reads in each sample), and Nitrosospira briensis-type OTU (NB_Bamo_01) predominated in all samples (except for OVA1 and OVA2, in which there were no bacterial amoA gene amplification) (Table S6). This result is in good accordance with 16S rRNA gene pyrotag analysis that found a Nitrosospira briensis-type OTU (no. 673) across the samples. An OTU (NB_Bamo_01) related to the Nitrosospira briensis strain Nsp10 (95.5% amoA gene sequence identity) was detected as a major AOB population in all niter-bed soils (Fig. 2 and Table S6). Nitrosospira briensis are enriched in and have been isolated from soil samples taken from sandy and agriculturally uncultivated areas of Europe [43]. To the best of our knowledge, only two reports have described the clear appearance of Nitrosospira briensis populations: water columns of the Chesapeake Bay [44] and soil samples of the Cascade Mountains in Oregon [45] in the U.S. Interestingly, Bollmann et al. [46] reported that under ammonia-starved conditions, the cells of Nitrosospira briensis had the ability to immediately recover ammonia oxidation activity upon exposure to ammonia-rich conditions. Although the mechanism behind this phenomenon is unclear, Nitrosospira briensis-type AOB may reserve their activity in ammonia-limited environments, such as the relict niter-bed soils. Within the genus Nitrosospira, an OTU (NB_Bamo_03) that is closely related to the Nitrosospira tenuis strain Nv-12 (96.2% sequence identity) was also detected in all bacterial amoA gene pytotag libraries; however, its ecophysiological traits (other than ammonia oxidation) remain unclear.

Bottom Line: The 16S rRNA gene pyrotag analysis showed that members of the phyla Proteobacteria, Actinobacteria, Bacteroidetes, Chloroflexi, Firmicutes, Gemmatimonadetes, and Planctomycetes were major microbial constituents, and principal coordinate analysis showed that the NO3-, Cl-, K+, and Na+ contents were potential determinants of the structures of entire microbial communities in relict niter-bed soils.Nitrososphaera"-type ammonia-oxidizing archaea (AOA), respectively, predominated in relict niter-bed soils.In addition, soil pH and organic carbon content were important factors for the ecological niche of AOB and AOA in relict niter-bed soil ecosystems.

View Article: PubMed Central - PubMed

Affiliation: Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Ibaraki, Japan.

ABSTRACT
From the 16th to the 18th centuries in Japan, saltpeter was produced using a biological niter-bed process and was formed under the floor of gassho-style houses in the historic villages of Shirakawa-go and Gokayama, which are classified as United Nations Educational, Scientific and Cultural Organization (UNESCO) World Heritage Sites. The relict niter-beds are now conserved in the underfloor space of gassho-style houses, where they are isolated from destabilizing environmental factors and retain the ability to produce nitrate. However, little is known about the nitrifying microbes in such relict niter-bed ecosystems. In this study, the microbial community structures within nine relict niter-bed soils were investigated using 454 pyrotag analysis targeting the 16S rRNA gene and the bacterial and archaeal ammonia monooxygenase gene (amoA). The 16S rRNA gene pyrotag analysis showed that members of the phyla Proteobacteria, Actinobacteria, Bacteroidetes, Chloroflexi, Firmicutes, Gemmatimonadetes, and Planctomycetes were major microbial constituents, and principal coordinate analysis showed that the NO3-, Cl-, K+, and Na+ contents were potential determinants of the structures of entire microbial communities in relict niter-bed soils. The bacterial and archaeal amoA libraries indicated that members of the Nitrosospira-type ammonia-oxidizing bacteria (AOB) and "Ca. Nitrososphaera"-type ammonia-oxidizing archaea (AOA), respectively, predominated in relict niter-bed soils. In addition, soil pH and organic carbon content were important factors for the ecological niche of AOB and AOA in relict niter-bed soil ecosystems.

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