Elsevier

Geoderma

Volume 358, 15 January 2020, 113979
Geoderma

Land-use legacy effects shape microbial contribution to N2O production in three tropical forests

https://doi.org/10.1016/j.geoderma.2019.113979Get rights and content

Highlights

  • AOA and nirS- and nirK-denitrifiers contribute to N2O production in tropical forests.

  • Land use legacies decreased AOA amoA, nirS, nirK and nosZ genes in reforested forest.

  • Land use legacy effects shape microbial contribution to soil N2O production.

Abstract

Soil microbes play a key role in regulating nitrous oxide (N2O) production, and land-use history can alter soil microbial communities. However, it remains unclear how land-use legacy effects shape soil nitrogen (N) transformation processes and microbial contribution to N2O production after long-term ecosystem recovery. To address this question, we measured soil N transformation processes and quantified the contribution of soil microbes to N2O production in three tropical forests with different land-use histories (primary, rehabilitated and disturbed forests) in South China. Results showed that soil N2O production was positively correlated with the abundances of ammonia-oxidizing archaea (AOA amoA) and nirS- and nirK-denitrifiers in the three forests, suggesting that these microbial groups can contribute greatly to N2O production in tropical forests, regardless of land-use legacy effects. However, the primary forest had higher microbial biomass, net N transformation rates and N2O production, and greater abundances of AOA and denitrifiers (nirS, nirK and nosZ) than those of both the disturbed and rehabilitated forests. These results suggest that land-use legacy effects can greatly alter N-cycling functional genes and N transformation processes, shaping soil N cycling in tropical forests.

Introduction

Nitrous oxide (N2O) is mainly produced and consumed through microbial nitrification and denitrification processes, and the balance between production and consumption determines net N2O fluxes (Chapuis-Lardy et al., 2007). Multiple microbial groups are responsible for N2O production, such as ammonia-oxidizing bacteria (AOB) and archaea (AOA) and denitrifying (nirS and nirK) bacteria (Braker and Conrad, 2011, Hu et al., 2015). Ammonia oxidation, the first rate-limiting step of nitrification, is performed by both AOA and AOB, which have been recognized as important contributors to soil N2O production (Hu et al., 2015, Hink et al., 2017). The reduction of nitrite (NO2) to nitric oxide (NO), the first gas-producing step of denitrification, is catalyzed by two structurally different but functionally equivalent nitrite reductases encoded by the nirK and nirS genes. These two functional genes have been widely used as potential indicators of soil N2O production (Morales et al., 2010, Petersen et al., 2012, Levy-Booth et al., 2014). In contrast, the nosZ-denitrifiers are mainly responsible for N2O consumption (Hu et al., 2015). The nosZ gene encodes N2O reductase, which catalyzes the reduction of N2O to N2 in the final step of denitrification.

Over the last several decades, many studies have demonstrated that previous land-use changes strongly affect soil nitrogen (N) cycling processes, especially N2O production (van Lent et al., 2015). For example, conversion of tropical primary forests to secondary forests and plantations decreased soil N availability and N2O production (Keller and Reiners, 1994, Verchot et al., 1999, Zhang et al., 2008), whereas conversion of tropical forests to agricultural lands increased N2O production (Van Lent et al., 2015, Gütlein et al., 2018). Moreover, previous land-use changes significantly altered soil microbial community composition (Fraterrigo et al., 2006, Jangid et al., 2011). A recent meta-analysis showed that conversion of primary forests to secondary forests and plantations decreased bacterial abundance and microbial biomass (Zhou et al., 2018). Land-use change is considered to be an important source of greenhouse gas emissions, with 7–18% of N2O emissions around the world generated from land-use change (van Lent et al., 2015). However, the microbial mechanisms for the previous land-use legacy effects on soil N2O production are poorly understood. To the best of our knowledge, there is limited information regarding the response of specific microbial functional groups to previous land-use changes in tropical forest ecosystems (see review by Pajares and Bohannan, 2016).

Our understanding of soil microbial communities responsible for N2O production and consumption is largely based on work in temperate and boreal forests, where soils are typically N limited (Levy-Booth et al., 2014, Pajares and Bohannan, 2016), although a few studies have investigated the soil microbial communities involved in N cycling in tropical and subtropical forests (Zhang et al., 2014, Lammel et al., 2015, Soper et al., 2018). In contrast to temperate/boreal forests, tropical forest soils are often highly weathered and acidic, with poor soil buffering capacity (Lu et al., 2014, Lu et al., 2015, Mao et al., 2017). In addition, soil N cycling in tropical forests is different from that in temperate/boreal forests because tropical forest soils are often N rich, with rapid N cycling rates (Martinelli et al., 1999, Matson et al., 1999). Therefore, microbial communities related to N2O production and consumption in tropical forests may be different from those in temperate/boreal forests. To date, however, it remains unclear on the link between soil net N2O production and specific microbial gene abundances such as ammonia oxidizers and denitrifiers in tropical forest ecosystems.

Over the past several centuries, many primary forests in China have been degraded by human activities, with only 2% of the total forests remaining intact (Liu et al., 2013a). Attempts to recover degraded forests have been made in many subtropical and tropical regions of China. During the early 1930s, large areas have been reforested with native pine species (e.g., Pinus massoniana) to prevent further land degradation (Mo et al., 2003, Mo et al., 1995). Although the cutting of trees is strictly prohibited, the harvesting of understory and litter is often allowed to satisfy fuel needs of local people. According to these practices, the reforested forests can be divided into disturbed forests (reforested with harvesting) and rehabilitated forests (reforested without harvesting) (Mo et al., 2003, Mo et al., 2006). These previous land-use changes may alter vegetation composition, soil chemistry and microbial communities, which in turn may affect soil N2O production. It is still unclear how land-use legacy effects shape soil N transformation processes and microbial contribution to N2O production after long-term ecosystem recovery.

In this study, we aim to explore the responses of soil N transformation processes and microbial contribution to N2O production to long-term land-use legacy effects in three tropical forests of southern China. We hypothesized that land-use legacy effects could alter microbial contribution to N2O production in tropical forests. Specially, we focus on 1) identifying which soil microbial functional groups contribute to the net N2O production, and 2) clarifying the underlying mechanisms responsible for the high N2O production. We mainly measured ammonia oxidizers (AOA amoA and AOB amoA) and denitrifiers (nirS, nirK and nosZ), because these microbial groups play a key role in forest ecosystem N cycling (Levy-Booth et al., 2014).

Section snippets

Study site and soil sampling

This study mainly focused on N-cycling functional genes, so we collected soil samples in January 2016 from each of three tropical forest types at the Dinghushan Biosphere Reserve (DBR), Guangdong Province, southern China (112°10′ E, 23°10′ N). The DBR has a monsoon climate and is located in a subtropical/tropical moist forest zone (Holdridge, 1967). The mean annual precipitation is 1927 mm, and the mean annual relative humidity is 80%. The mean annual temperature is 21.0 °C, with the coldest

Soil general properties and soil microbial biomass

At the beginning of incubation (day 0), the total C, total N, available N (mainly as NO3) and MBN contents and soil field capacity exhibited the following trend: rehabilitated forest < disturbed forest < primary forest (Fig. 1; Table 1). For example, the total C, total N and NO3 contents in the primary forest were 1.1, 1.3 and 3.2 times higher than those in the rehabilitated forest, and 60%, 62% and 134% higher than those in the disturbed forest, respectively. Soil MBN in the primary forest

Discussion

We found that the net N2O production was higher in the primary forest than in the reforested forest (disturbed and rehabilitated forests), which was consistent with the findings of previous studies (e.g., Keller and Reiners, 1994, Verchot et al., 1999, Tang et al., 2006, Zhang et al., 2008). These patterns can be largely attributed to the legacy effects of previous land-use history (e.g. forest clear-cutting), which can greatly alter soil microbial structure and the related processes (

Conclusion

In this study, we addressed how land-use legacy effects shaped soil microbial contribution to N2O production in three tropical forests. We found that both abiotic (moisture and substrate availability) and biotic (microbial biomass and N-cycling functional gene abundance) factors could determine soil N2O production. Overall, we clarified that ammonia-oxidizing archaea (AOA) and nirS- and nirK-denitrifiers played an important role in regulating N2O production in all the studied tropical forests,

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper

Acknowledgments

We would like to thank Hui-Xuan Liao for her help with statistical analysis. We greatly appreciate the editor and two anonymous reviews for their valuable comments and suggestions. The study was supported by the National Natural Science Foundation of China (31030015), the Science and Technology Planning Project of Guangzhou (201607020027) and Guangdong (2018A030321013), the Pearl River S&T Nova Program of Guangzhou (201806010150), the Special Funds of Guangdong Province for Promoting Economic

References (90)

  • K. Jangid et al.

    Land-use history has a stronger impact on soil microbial community composition than aboveground vegetation and soil properties

    Soil Biol. Biochem.

    (2011)
  • R.G. Joergensen et al.

    Ninhydrin-reactive nitrogen measurements of microbial biomass in 0.5 M K2SO4 soil extracts

    Soil Biol. Biochem.

    (1990)
  • D.J. Levy-Booth et al.

    Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems

    Soil Biol. Biochem.

    (2014)
  • X. Liu et al.

    Soil environmental factors rather than denitrification gene abundance control N2O fluxes in a wet sclerophyll forest with different burning frequency

    Soil Biol. Biochem.

    (2013)
  • Q. Mao et al.

    Effects of long-term nitrogen and phosphorus additions on soil acidification in an N-rich tropical forest

    Geoderma

    (2017)
  • H. Meng et al.

    A comparison of denitrifying bacterial community structures and abundance in acidic soils between natural forest and re-vegetated forest of Nanling Nature Reserve in southern China

    J. Environ. Manage.

    (2017)
  • J. Mo et al.

    Nitrogen availability in disturbed, rehabilitated and mature forests of tropical China

    Forest Ecol. Manage.

    (2003)
  • J.S. Norman et al.

    Substrate and nutrient limitation of ammonia-oxidizing bacteria and archaea in temperate forest soil

    Soil Biol. Biochem.

    (2014)
  • Y. Ouyang et al.

    Effect of nitrogen fertilization on the abundance of nitrogen cycling genes in agricultural soils: a meta-analysis of field studies

    Soil Biol. Biochem.

    (2018)
  • X. Ouyang et al.

    Effect of N and P addition on soil organic C potential mineralization in forest soils in South China

    J. Environ. Sci.

    (2008)
  • J.T. Richardson

    Eta squared and partial eta squared as measures of effect size in educational research

    Educ. Res. Rev.

    (2011)
  • M. Spohn et al.

    Soil microbial carbon use efficiency and biomass turnover in a long-term fertilization experiment in a temperate grassland

    Soil Biol. Biochem.

    (2016)
  • Y. Tang et al.

    Impacts of nitrogen and phosphorus additions on the abundance and community structure of ammonia oxidizers and denitrifying bacteria in Chinese fir plantations

    Soil Biol. Biochem.

    (2016)
  • E.D. Vance et al.

    An extraction method for measuring soil microbial biomass

    Soil Biol. Biochem.

    (1987)
  • E. Vance et al.

    Substrate limitations to microbial activity in taiga forest floors

    Soil Biol. Biochem.

    (2001)
  • X. Wang et al.

    Long-term fertilization effects on active ammonia oxidizers in an acidic upland soil in China

    Soil Biol. Biochem.

    (2015)
  • J. Zhang et al.

    N2O production pathways in the subtropical acid forest soils in China

    Environ. Res.

    (2011)
  • M. Zheng et al.

    Different responses of asymbiotic nitrogen fixation to nitrogen addition between disturbed and rehabilitated subtropical forests

    Sci. Total Environ.

    (2017)
  • R.D. Bowden et al.

    Effects of nitrogen additions on annual nitrous oxide fluxes from temperate forest soils in the northeastern United States

    J. Geophys. Res. Atmos.

    (1991)
  • S.A. Boyle-Yarwood et al.

    Community composition of ammonia-oxidizing bacteria and archaea in soils under stands of red alder and Douglas fir in Oregon

    Environ. Microbiol.

    (2008)
  • S.W. Buol et al.

    Soil Genesis and Classification

    (2011)
  • L. Chapuis-Lardy et al.

    Soils, a sink for N2O? A review

    Global Change Biol.

    (2007)
  • B. Chen et al.

    Differential responses of invasive and native plants to warming with simulated changes in diurnal temperature ranges

    Aob Plants

    (2017)
  • A.M. De Carvalho et al.

    Soil N2O fluxes in integrated production systems, continuous pasture and Cerrado

    Nutr. Cycl. Agroecosys.

    (2017)
  • T.A. Doane et al.

    Spectrophotometric determination of nitrate with a single reagent

    Anal. Lett.

    (2003)
  • J. Durán et al.

    Changes in net N mineralization rates and soil N and P pools in a pine forest wildfire chronosequence

    Biol. Fert. Soils

    (2009)
  • Y.T. Fang et al.

    Dynamics of soil inorganic nitrogen and their responses to nitrogen additions in three subtropical forests, south China

    J. Environ. Sci.

    (2006)
  • J.M. Fraterrigo et al.

    Microbial community variation and its relationship with nitrogen mineralization in historically altered forests

    Ecology

    (2006)
  • D.C. Garcia-Montiel et al.

    Carbon limitations to nitrous oxide emissions in a humid tropical forest of the Brazilian Amazon

    Biol. Fert. Soils

    (2003)
  • D.R. Graf et al.

    Intergenomic comparisons highlight modularity of the denitrification pathway and underpin the importance of community structure for N2O emissions

    PLoS One

    (2014)
  • C. Gubry-Rangin et al.

    Archaea rather than bacteria control nitrification in two agricultural acidic soils

    FEMS Microbiol. Ecol.

    (2010)
  • A. Gütlein et al.

    Impacts of climate and land use on N2O and CH4 fluxes from tropical ecosystems in the Mt. Kilimanjaro region, Tanzania

    Global Change Biol.

    (2018)
  • S.J. Hall et al.

    Nitrogen oxide emissions after nitrogen additions in tropical forests

    Nature

    (1999)
  • S. Hallin et al.

    Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment

    ISME J.

    (2009)
  • R. Hatzenpichler

    Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea

    Appl. Environ. Microbiol.

    (2012)
  • Cited by (0)

    View full text