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
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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)