Evolution of trees and mycorrhizal fungi intensifies silicate mineral weathering

Biology Letters, Dec 2012

Forested ecosystems diversified more than 350 Ma to become major engines of continental silicate weathering, regulating the Earth's atmospheric carbon dioxide concentration by driving calcium export into ocean carbonates. Our field experiments with mature trees demonstrate intensification of this weathering engine as tree lineages diversified in concert with their symbiotic mycorrhizal fungi. Preferential hyphal colonization of the calcium silicate-bearing rock, basalt, progressively increased with advancement from arbuscular mycorrhizal (AM) to later, independently evolved ectomycorrhizal (EM) fungi, and from gymnosperm to angiosperm hosts with both fungal groups. This led to ‘trenching’ of silicate mineral surfaces by AM and EM fungi, with EM gymnosperms and angiosperms releasing calcium from basalt at twice the rate of AM gymnosperms. Our findings indicate mycorrhiza-driven weathering may have originated hundreds of millions of years earlier than previously recognized and subsequently intensified with the evolution of trees and mycorrhizas to affect the Earth's long-term CO2 and climate history.

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Evolution of trees and mycorrhizal fungi intensifies silicate mineral weathering

Joe Quirk ) David J. Beerling Steve A. Banwart Gabriella Kakonyi Maria E. Romero-Gonzalez Jonathan R. Leake 0 Kroto Research Institute, University of Sheffield , North Campus, Sheffield S3 7HQ, UK 1 Department of Animal and Plant Sciences, University of Sheffield , Sheffield, S10 2TN, UK Articles on similar topics can be found in the following collections biochemistry (21 articles) environmental science (160 articles) evolution (787 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top right-hand corner of the article or click here References Subject collections Email alerting service Biol. Lett. (2012) 8, 10061011 doi:10.1098/rsbl.2012.0503 Published online 1 August 2012 Global change biology Evolution of trees and mycorrhizal fungi intensifies silicate mineral weathering Joe Quirk1,*, David J. Beerling1, Steve A. Banwart2, Gabriella Kakonyi2, Maria E. Romero-Gonzalez2 and Jonathan R. Leake1 Forested ecosystems diversified more than 350 Ma to become major engines of continental silicate weathering, regulating the Earths atmospheric carbon dioxide concentration by driving calcium export into ocean carbonates. Our field experiments with mature trees demonstrate intensification of this weathering engine as tree lineages diversified in concert with their symbiotic mycorrhizal fungi. Preferential hyphal colonization of the calcium silicate-bearing rock, basalt, progressively increased with advancement from arbuscular mycorrhizal (AM) to later, independently evolved ectomycorrhizal (EM) fungi, and from gymnosperm to angiosperm hosts with both fungal groups. This led to trenching of silicate mineral surfaces by AM and EM fungi, with EM gymnosperms and angiosperms releasing calcium from basalt at twice the rate of AM gymnosperms. Our findings indicate mycorrhiza-driven weathering may have originated hundreds of millions of years earlier than previously recognized and subsequently intensified with the evolution of trees and mycorrhizas to affect the Earths long-term CO2 and climate history. 1. INTRODUCTION Forested ecosystems are major engines of biological weathering in terrestrial environments, but we know almost nothing about how the strength of these engines changed as tree lineages and their root-associating fungal symbionts evolved. Fossil roots of early gymnosperms from at least the Carboniferous are colonized by arbuscular mycorrhizal (AM) fungi, and this type of mycorrhiza continues to be found in the vast majority of tree species, including in most of the more recently evolved angiosperm taxa [1]. Independently evolving ectomycorrhizal (EM) fungi diversified from the Cretaceous, forming mycorrhizal associations with the Pinaceae and angiosperm trees in the Betulaceae and Fagaceae that now dominate temperate and boreal Electronic supplementary material is available at http://dx.doi.org/ 10.1098/rsbl.2012.0503 or via http://rsbl.royalsocietypublishing.org. forests, as well as with angiosperm trees in the Myrtaceae, Fabaceae and Dipterocarpaceae, that can form dominant stands in warm temperate and tropical regions [1,2]. Both mycorrhizal types use host photosynthate to support extensive hyphal networks with high absorptive surface area for nutrient element mass transfer from the substrate. In trees forming AM, root functioning is augmented by the nutrientscavenging activities of the fungi, whereas EM fungi completely envelop tree root tips to subsume the soil root interface. EM fungi thereby control the translocation of elements from soil to tree and can also enhance mineral weathering through exudation of low molecular weight organic compounds [3,4]. Here, we address the primary hypothesis that functional differences between mycorrhizal types, coupled with the evolution of their host trees, drives intensification of silicate weathering. We used mature tree taxa with crown diversification ages ranging from tens to hundreds of millions of years (figure 1a and table 1) in conjunction with a suite of methods isolating mycorrhizal hyphal effects on mineral weathering by excluding tree roots with mesh bags [8]. The extant gymnosperm taxa available for these studies may be only approximate representatives of the ancestral taxa that dominated temperate forests before the rise to dominance of angiosperms [6,9]. Stem- and crownnode ages estimated with molecular clocks suggest gymnosperms evolved and adapted over the same evolutionary time span as their sister lineages, the angiosperms (table 1) [6]. Mycorrhiza-driven weathering was quantified by burying uniform-sized grains of silicate rocks that are either calcium-rich (basalt) or -poor (granite), along with quartz controls (see the electronic supplementary material, tables S1 and S2). Weathering of calcium from silicates plays a major role in regulating atmospheric CO2 on geological timescales [10,11] by promoting the deposition of marine calcium carbonates. Our field studies control for climate and soi (...truncated)


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Joe Quirk, David J. Beerling, Steve A. Banwart, Gabriella Kakonyi, Maria E. Romero-Gonzalez, Jonathan R. Leake. Evolution of trees and mycorrhizal fungi intensifies silicate mineral weathering, Biology Letters, 2012, pp. 1006-1011, 8/6, DOI: 10.1098/rsbl.2012.0503