Long-term warming in Alaska enlarges the diazotrophic community in deep soils

Jiajie Feng, Christopher Penton, Zhili He, Joy D. Van Nostrand, Mengting M. Yuan, Liyou Wu, Cong Wang, Yujia Qin, Zhou J. Shi, Xue Guo, Edward A.G. Schuur, Yiqi Luo, Rosvel Bracho, Konstantinos T. Konstantinidis, James R. Cole, James M. Tiedje, Yunfeng Yang, Jizhong Zhou

Research output: Contribution to journalArticle

Abstract

Tundra ecosystems are typically carbon (C) rich but nitrogen (N) limited. Since biological N 2 fixation is the major source of biologically available N, the soil N 2 -fixing (i.e., diazotrophic) community serves as an essential N supplier to the tundra ecosystem. Recent climate warming has induced deeper permafrost thaw and adversely affected C sequestration, which is modulated by N availability. Therefore, it is crucial to examine the responses of diazotrophic communities to warming across the depths of tundra soils. Herein, we carried out one of the deepest sequencing efforts of nitrogenase gene (nifH) to investigate how 5 years of experimental winter warming affects Alaskan soil diazotrophic community composition and abundance spanning both the organic and mineral layers. Although soil depth had a stronger influence on diazotrophic community composition than warming, warming significantly (P < 0.05) enhanced diazotrophic abundance by 86.3% and aboveground plant biomass by 25.2%. Diazotrophic composition in the middle and lower organic layers, detected by nifH sequencing and a microarray-based tool (GeoChip), was markedly altered, with an increase of α-diversity. Changes in diazotrophic abundance and composition significantly correlated with soil moisture, soil thaw duration, and plant biomass, as shown by structural equation modeling analyses. Therefore, more abundant diazotrophic communities induced by warming may potentially serve as an important mechanism for supplementing biologically available N in this tundra ecosystem. IMPORTANCE With the likelihood that changes in global climate will adversely affect the soil C reservoir in the northern circumpolar permafrost zone, an understanding of the potential role of diazotrophic communities in enhancing biological N 2 fixation, which constrains both plant production and microbial decomposition in tundra soils, is important in elucidating the responses of soil microbial communities to global climate change. A recent study showed that the composition of the diazotrophic community in a tundra soil exhibited no change under a short-term (1.5-year) winter warming experiment. However, it remains crucial to examine whether the lack of diazotrophic community responses to warming is persistent over a longer time period as a possibly important mechanism in stabilizing tundra soil C. Through a detailed characterization of the effects of winter warming on diazotrophic communities, we showed that a long-term (5-year) winter warming substantially enhanced diazotrophic abundance and altered community composition, though soil depth had a stronger influence on diazotrophic community composition than warming. These changes were best explained by changes in soil moisture, soil thaw duration, and plant biomass. These results provide crucial insights into the potential factors that may impact future C and N availability in tundra regions.

Original languageEnglish (US)
Article numbere02521-18
JournalmBio
Volume10
Issue number1
DOIs
StatePublished - Jan 1 2019

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Soil
Biomass
Ecosystem
Climate
Nitrogenase
High-Throughput Nucleotide Sequencing
Tundra
Climate Change
Minerals
Nitrogen
Carbon

Keywords

  • Climate warming
  • Diazotrophs
  • Gene sequencing
  • Soil microbiology
  • Tundra

ASJC Scopus subject areas

  • Microbiology
  • Virology

Cite this

Feng, J., Penton, C., He, Z., Van Nostrand, J. D., Yuan, M. M., Wu, L., ... Zhou, J. (2019). Long-term warming in Alaska enlarges the diazotrophic community in deep soils. mBio, 10(1), [e02521-18]. https://doi.org/10.1128/mBio.02521-18

Long-term warming in Alaska enlarges the diazotrophic community in deep soils. / Feng, Jiajie; Penton, Christopher; He, Zhili; Van Nostrand, Joy D.; Yuan, Mengting M.; Wu, Liyou; Wang, Cong; Qin, Yujia; Shi, Zhou J.; Guo, Xue; Schuur, Edward A.G.; Luo, Yiqi; Bracho, Rosvel; Konstantinidis, Konstantinos T.; Cole, James R.; Tiedje, James M.; Yang, Yunfeng; Zhou, Jizhong.

In: mBio, Vol. 10, No. 1, e02521-18, 01.01.2019.

Research output: Contribution to journalArticle

Feng, J, Penton, C, He, Z, Van Nostrand, JD, Yuan, MM, Wu, L, Wang, C, Qin, Y, Shi, ZJ, Guo, X, Schuur, EAG, Luo, Y, Bracho, R, Konstantinidis, KT, Cole, JR, Tiedje, JM, Yang, Y & Zhou, J 2019, 'Long-term warming in Alaska enlarges the diazotrophic community in deep soils', mBio, vol. 10, no. 1, e02521-18. https://doi.org/10.1128/mBio.02521-18
Feng, Jiajie ; Penton, Christopher ; He, Zhili ; Van Nostrand, Joy D. ; Yuan, Mengting M. ; Wu, Liyou ; Wang, Cong ; Qin, Yujia ; Shi, Zhou J. ; Guo, Xue ; Schuur, Edward A.G. ; Luo, Yiqi ; Bracho, Rosvel ; Konstantinidis, Konstantinos T. ; Cole, James R. ; Tiedje, James M. ; Yang, Yunfeng ; Zhou, Jizhong. / Long-term warming in Alaska enlarges the diazotrophic community in deep soils. In: mBio. 2019 ; Vol. 10, No. 1.
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abstract = "Tundra ecosystems are typically carbon (C) rich but nitrogen (N) limited. Since biological N 2 fixation is the major source of biologically available N, the soil N 2 -fixing (i.e., diazotrophic) community serves as an essential N supplier to the tundra ecosystem. Recent climate warming has induced deeper permafrost thaw and adversely affected C sequestration, which is modulated by N availability. Therefore, it is crucial to examine the responses of diazotrophic communities to warming across the depths of tundra soils. Herein, we carried out one of the deepest sequencing efforts of nitrogenase gene (nifH) to investigate how 5 years of experimental winter warming affects Alaskan soil diazotrophic community composition and abundance spanning both the organic and mineral layers. Although soil depth had a stronger influence on diazotrophic community composition than warming, warming significantly (P < 0.05) enhanced diazotrophic abundance by 86.3{\%} and aboveground plant biomass by 25.2{\%}. Diazotrophic composition in the middle and lower organic layers, detected by nifH sequencing and a microarray-based tool (GeoChip), was markedly altered, with an increase of α-diversity. Changes in diazotrophic abundance and composition significantly correlated with soil moisture, soil thaw duration, and plant biomass, as shown by structural equation modeling analyses. Therefore, more abundant diazotrophic communities induced by warming may potentially serve as an important mechanism for supplementing biologically available N in this tundra ecosystem. IMPORTANCE With the likelihood that changes in global climate will adversely affect the soil C reservoir in the northern circumpolar permafrost zone, an understanding of the potential role of diazotrophic communities in enhancing biological N 2 fixation, which constrains both plant production and microbial decomposition in tundra soils, is important in elucidating the responses of soil microbial communities to global climate change. A recent study showed that the composition of the diazotrophic community in a tundra soil exhibited no change under a short-term (1.5-year) winter warming experiment. However, it remains crucial to examine whether the lack of diazotrophic community responses to warming is persistent over a longer time period as a possibly important mechanism in stabilizing tundra soil C. Through a detailed characterization of the effects of winter warming on diazotrophic communities, we showed that a long-term (5-year) winter warming substantially enhanced diazotrophic abundance and altered community composition, though soil depth had a stronger influence on diazotrophic community composition than warming. These changes were best explained by changes in soil moisture, soil thaw duration, and plant biomass. These results provide crucial insights into the potential factors that may impact future C and N availability in tundra regions.",
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TY - JOUR

T1 - Long-term warming in Alaska enlarges the diazotrophic community in deep soils

AU - Feng, Jiajie

AU - Penton, Christopher

AU - He, Zhili

AU - Van Nostrand, Joy D.

AU - Yuan, Mengting M.

AU - Wu, Liyou

AU - Wang, Cong

AU - Qin, Yujia

AU - Shi, Zhou J.

AU - Guo, Xue

AU - Schuur, Edward A.G.

AU - Luo, Yiqi

AU - Bracho, Rosvel

AU - Konstantinidis, Konstantinos T.

AU - Cole, James R.

AU - Tiedje, James M.

AU - Yang, Yunfeng

AU - Zhou, Jizhong

PY - 2019/1/1

Y1 - 2019/1/1

N2 - Tundra ecosystems are typically carbon (C) rich but nitrogen (N) limited. Since biological N 2 fixation is the major source of biologically available N, the soil N 2 -fixing (i.e., diazotrophic) community serves as an essential N supplier to the tundra ecosystem. Recent climate warming has induced deeper permafrost thaw and adversely affected C sequestration, which is modulated by N availability. Therefore, it is crucial to examine the responses of diazotrophic communities to warming across the depths of tundra soils. Herein, we carried out one of the deepest sequencing efforts of nitrogenase gene (nifH) to investigate how 5 years of experimental winter warming affects Alaskan soil diazotrophic community composition and abundance spanning both the organic and mineral layers. Although soil depth had a stronger influence on diazotrophic community composition than warming, warming significantly (P < 0.05) enhanced diazotrophic abundance by 86.3% and aboveground plant biomass by 25.2%. Diazotrophic composition in the middle and lower organic layers, detected by nifH sequencing and a microarray-based tool (GeoChip), was markedly altered, with an increase of α-diversity. Changes in diazotrophic abundance and composition significantly correlated with soil moisture, soil thaw duration, and plant biomass, as shown by structural equation modeling analyses. Therefore, more abundant diazotrophic communities induced by warming may potentially serve as an important mechanism for supplementing biologically available N in this tundra ecosystem. IMPORTANCE With the likelihood that changes in global climate will adversely affect the soil C reservoir in the northern circumpolar permafrost zone, an understanding of the potential role of diazotrophic communities in enhancing biological N 2 fixation, which constrains both plant production and microbial decomposition in tundra soils, is important in elucidating the responses of soil microbial communities to global climate change. A recent study showed that the composition of the diazotrophic community in a tundra soil exhibited no change under a short-term (1.5-year) winter warming experiment. However, it remains crucial to examine whether the lack of diazotrophic community responses to warming is persistent over a longer time period as a possibly important mechanism in stabilizing tundra soil C. Through a detailed characterization of the effects of winter warming on diazotrophic communities, we showed that a long-term (5-year) winter warming substantially enhanced diazotrophic abundance and altered community composition, though soil depth had a stronger influence on diazotrophic community composition than warming. These changes were best explained by changes in soil moisture, soil thaw duration, and plant biomass. These results provide crucial insights into the potential factors that may impact future C and N availability in tundra regions.

AB - Tundra ecosystems are typically carbon (C) rich but nitrogen (N) limited. Since biological N 2 fixation is the major source of biologically available N, the soil N 2 -fixing (i.e., diazotrophic) community serves as an essential N supplier to the tundra ecosystem. Recent climate warming has induced deeper permafrost thaw and adversely affected C sequestration, which is modulated by N availability. Therefore, it is crucial to examine the responses of diazotrophic communities to warming across the depths of tundra soils. Herein, we carried out one of the deepest sequencing efforts of nitrogenase gene (nifH) to investigate how 5 years of experimental winter warming affects Alaskan soil diazotrophic community composition and abundance spanning both the organic and mineral layers. Although soil depth had a stronger influence on diazotrophic community composition than warming, warming significantly (P < 0.05) enhanced diazotrophic abundance by 86.3% and aboveground plant biomass by 25.2%. Diazotrophic composition in the middle and lower organic layers, detected by nifH sequencing and a microarray-based tool (GeoChip), was markedly altered, with an increase of α-diversity. Changes in diazotrophic abundance and composition significantly correlated with soil moisture, soil thaw duration, and plant biomass, as shown by structural equation modeling analyses. Therefore, more abundant diazotrophic communities induced by warming may potentially serve as an important mechanism for supplementing biologically available N in this tundra ecosystem. IMPORTANCE With the likelihood that changes in global climate will adversely affect the soil C reservoir in the northern circumpolar permafrost zone, an understanding of the potential role of diazotrophic communities in enhancing biological N 2 fixation, which constrains both plant production and microbial decomposition in tundra soils, is important in elucidating the responses of soil microbial communities to global climate change. A recent study showed that the composition of the diazotrophic community in a tundra soil exhibited no change under a short-term (1.5-year) winter warming experiment. However, it remains crucial to examine whether the lack of diazotrophic community responses to warming is persistent over a longer time period as a possibly important mechanism in stabilizing tundra soil C. Through a detailed characterization of the effects of winter warming on diazotrophic communities, we showed that a long-term (5-year) winter warming substantially enhanced diazotrophic abundance and altered community composition, though soil depth had a stronger influence on diazotrophic community composition than warming. These changes were best explained by changes in soil moisture, soil thaw duration, and plant biomass. These results provide crucial insights into the potential factors that may impact future C and N availability in tundra regions.

KW - Climate warming

KW - Diazotrophs

KW - Gene sequencing

KW - Soil microbiology

KW - Tundra

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