Effects of Long-Term CO2 Enrichment on Soil-Atmosphere CH4 Fluxes and the Spatial Micro-Distribution of Methanotrophic Bacteria

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Abstract

Background

Effects of elevated atmospheric CO ₂ concentrations on plant growth and associated C cycling have intensively been studied, but less is known about effects on the fluxes of radiatively active trace gases other than CO ₂. Net soil-atmosphere CH ₄ fluxes are determined by the balance of soil microbially-driven methane (CH ₄) oxidation and methanogenesis, and both might change under elevated CO ₂.

Methods and Results

Here, we studied CH ₄ dynamics in a permanent grassland exposed to elevated CO ₂ for 14 years. Soil-atmosphere fluxes of CH ₄ were measured using large static chambers, over a period of four years. The ecosystem was a net sink for atmospheric CH ₄ for most of the time except summer to fall when net CH ₄ emissions occurred. We did not detect any elevated CO ₂ effects on CH ₄ fluxes, but emissions were difficult to quantify due to their discontinuous nature, most likely because of ebullition from the saturated zone. Potential methanotrophic activity, determined by incubation of fresh sieved soil under standardized conditions, also did not reveal any effect of the CO ₂ treatment. Finally, we determined the spatial micro-distribution of methanotrophic activity at less than 5× atmospheric (10 ppm) and elevated (10000 ppm) CH ₄ concentrations, using a novel auto-radiographic technique. These analyses indicated that domains of net CH ₄ assimilation were distributed throughout the analyzed top 15 cm of soils, with no dependence on CH ₄ concentration or CO ₂ treatment.

Conclusions

Our investigations suggest that elevated CO ₂ exerts no or only minor effects on CH ₄ fluxes in the type of ecosystem we studied, at least as long as soil moisture differences are small or absent as was the case here. The autoradiographic analyses further indicate that the spatial niche of CH ₄ oxidation does not shift in response to CO ₂ enrichment or CH ₄ concentration, and that the same type of methanotrophs may oxidize CH ₄ from atmospheric and soil-internal sources.

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Most cited references 14

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Methane emissions from terrestrial plants under aerobic conditions.

Frank Keppler, John T G Hamilton, Marc Brass … (2006)

Methane is an important greenhouse gas and its atmospheric concentration has almost tripled since pre-industrial times. It plays a central role in atmospheric oxidation chemistry and affects stratospheric ozone and water vapour levels. Most of the methane from natural sources in Earth's atmosphere is thought to originate from biological processes in anoxic environments. Here we demonstrate using stable carbon isotopes that methane is readily formed in situ in terrestrial plants under oxic conditions by a hitherto unrecognized process. Significant methane emissions from both intact plants and detached leaves were observed during incubation experiments in the laboratory and in the field. If our measurements are typical for short-lived biomass and scaled on a global basis, we estimate a methane source strength of 62-236 Tg yr(-1) for living plants and 1-7 Tg yr(-1) for plant litter (1 Tg = 10(12) g). We suggest that this newly identified source may have important implications for the global methane budget and may call for a reconsideration of the role of natural methane sources in past climate change.

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Nitrogen as a regulatory factor of methane oxidation in soils and sediments.

Paul L E Bodelier, Hendrikus Laanbroek (2004)

The oxidation of methane by methane-oxidising microorganisms is an important link in the global methane budget. Oxic soils are a net sink while wetland soils are a net source of atmospheric methane. It has generally been accepted that the consumption of methane in upland as well as lowland systems is inhibited by nitrogenous fertiliser additions. Hence, mineral nitrogen (i.e. ammonium/nitrate) has conceptually been treated as a component with the potential to enhance emission of methane from soils and sediments to the atmosphere, and results from numerous studies have been interpreted as such. Recently, ammonium-based fertilisation was demonstrated to stimulate methane consumption in rice paddies. Growth and activity of methane-consuming bacteria in microcosms as well as in natural rice paddies was N limited. Analysing the available literature revealed that indications for N limitation of methane consumption have been reported in a variety of lowland soils, upland soils, and sediments. Obviously, depriving methane-oxidising bacteria of a suitable source of N hampers their growth and activity. However, an almost instantaneous link between the presence of mineral nitrogen (i.e. ammonium, nitrate) and methane-oxidising activity, as found in rice soils and culture experiments, requires an alternative explanation. We propose that switching from mineral N assimilation to the fixation of molecular nitrogen may explain this phenomenon. However, there is as yet no experimental evidence for any mechanism of instantaneous stimulation, since most studies have assumed that nitrogenous fertiliser is inhibitory of methane oxidation in soils and have focused only on this aspect. Nitrogen as essential factor on the sink side of the global methane budget has been neglected, leading to erroneous interpretation of methane emission dynamics, especially from wetland environments. The purpose of this minireview is to summarise and balance the data on the regulatory role of nitrogen in the consumption of methane by soils and sediments, and thereby stimulate the scientific community to embark on experiments to close the existing gap in knowledge.

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Water relations in grassland and desert ecosystems exposed to elevated atmospheric CO2.

D Pataki, Pascal A. Niklaus, H. Polley … (2004)

Atmospheric CO2 enrichment may stimulate plant growth directly through (1) enhanced photosynthesis or indirectly, through (2) reduced plant water consumption and hence slower soil moisture depletion, or the combination of both. Herein we describe gas exchange, plant biomass and species responses of five native or semi-native temperate and Mediterranean grasslands and three semi-arid systems to CO2 enrichment, with an emphasis on water relations. Increasing CO2 led to decreased leaf conductance for water vapor, improved plant water status, altered seasonal evapotranspiration dynamics, and in most cases, periodic increases in soil water content. The extent, timing and duration of these responses varied among ecosystems, species and years. Across the grasslands of the Kansas tallgrass prairie, Colorado shortgrass steppe and Swiss calcareous grassland, increases in aboveground biomass from CO2 enrichment were relatively greater in dry years. In contrast, CO2-induced aboveground biomass increases in the Texas C3/C4 grassland and the New Zealand pasture seemed little or only marginally influenced by yearly variation in soil water, while plant growth in the Mojave Desert was stimulated by CO2 in a relatively wet year. Mediterranean grasslands sometimes failed to respond to CO2-related increased late-season water, whereas semiarid Negev grassland assemblages profited. Vegetative and reproductive responses to CO2 were highly varied among species and ecosystems, and did not generally follow any predictable pattern in regard to functional groups. Results suggest that the indirect effects of CO2 on plant and soil water relations may contribute substantially to experimentally induced CO2-effects, and also reflect local humidity conditions. For landscape scale predictions, this analysis calls for a clear distinction between biomass responses due to direct CO2 effects on photosynthesis and those indirect CO2 effects via soil moisture as documented here.

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Author and article information

Contributors

Riikka Rinnan: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, CA USA )

ISSN (Electronic): 1932-6203

Publication date (Electronic): 6 July 2015

Publication date Collection: 2015

Volume: 10

Issue: 7

Electronic Location Identifier: e0131665

Affiliations

[1 ]Institute of Evolutionary Biology and Environmental Studies, University of Zürich, Zürich, Switzerland

[2 ]Institute of Plant Ecology, Justus-Liebig-University, Giessen, Germany

[3 ]Climate Change Research for Special Crops, Hochschule Geisenheim University, Geisenheim, Germany

University of Copenhagen, DENMARK

Author notes

Competing Interests: The authors have declared that no competing interests exist.

Conceived and designed the experiments: PAN CIK. Performed the experiments: SK CG. Analyzed the data: SK CG PAN. Wrote the paper: SK CG CIK PAN.

* E-mail: Pascal.Niklaus@ 123456ieu.uzh.ch (PN); Claudia.Kamman@ 123456hs-gm.de (CK)

Article

Publisher ID: PONE-D-15-13676

DOI: 10.1371/journal.pone.0131665

PMC ID: 4492808

PubMed ID: 26147694

SO-VID: 4eda0cb1-27ac-474a-8428-1bc6bebd7b1c

License:

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

History

Date received : 7 April 2015

Date accepted : 4 June 2015

Page count

Figures: 7, Tables: 1, Pages: 14

Funding

SK has been funded by a stipend of Aga Khan Foundation. PAN supported the study from regular funds from the University of Zurich. The Hessian Agency for the Environment and Geology (HLUG) contributed to the running costs of the Giessen Free Air CO2 Enrichment. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Custom metadata

Data Availability All relevant data are within the paper and its Supporting Information files.