Community-level traits as a way to partly circumvent the
culturing problem in mycorrhizal trait-based ecology?
Chagnon, P.-L.
Data availability statement: No new data has been generated in
this manuscript.
Traits are the intermediate by which species respond to environmental
filters and influence ecosystem functions. With the myriad of
biogeochemical processes controlled by fungi, the past decade has
witnessed a rising interest in applying trait-based approaches, core to
the toolkit of plant and animal ecophysiologists, to fungi. One of the
first challenges to tackle when working on fungal ecophysiology is to
circumscribe the very definition of what we consider a fungal trait.
Traits are characteristics/features possessed by an individualthat can influence how it interacts with its environment. Here the
individual scale is both important, and problematic. Important because
the very goal of comparative ecology is to measure traits on individuals
belonging to known species. This allows to populate trait databases, and
syntheses of such databases can reveal key trade-offs and trait
syndromes that govern species’ life-histories. The scale of the
individual is problematic, however, because it is hard to define for
soil fungi, and because a rare minority of fungi can be sampled at the
individual scale in the environment (e.g., macroscopic sporocarps,
ectomycorrhizal root tips, lichen thalli). Beyond this minority, the
individual organisms can only be accessed/sampled through establishing
fungal cultures, which probably represents one of the main bottlenecks
in the development of fungal trait databases. In this issue, Zhang et
al. (2022) show how interesting insights in fungal trait-based ecology
can be gained by working at the community level.
In their study, Zhang et al. (2022) adapted a protocol developed by
Neumann & George (2005) to capture mycorrhizal fungal hyphae using
ingrowth bags. If we assume that most hyphae recovered through this
technique are mycorrhizal, the washed hyphae can be characterized
through various chemical/morphological downstream analyses. Measuring
such traits for biomass recovered from whole communities is akin to
estimating community-weighted mean (CWM) traits, which are central to
many aspects of ecophysiology. Various paradigms/theories in community
ecology assume some form of equilibrium between species and their
environment (Leibold et al., 2004). If we assume (1) a heterogeneous
environment, (2) species as reproductively isolated units competing for
space/resources and (3) traits as determinants of their reproductive
success, correlations between species traits and environmental
parameters are naturally expected to arise (Shipley et al., 2011). Under
specific stable environmental conditions, a species bearing certain
traits should have a higher probability to (1) occur and (2) become
abundant in such environment. At the community level, we thus expect a
correlation between CWM traits (the sum of species mean traits weighted
by their relative abundances), and environmental parameters (box 1).
With mycorrhizal fungi, we can have a reasonable access to species’
relative abundances through sequence-based profiles of communities, but
the species × traits matrix remains inaccessible. The shortcut taken by
Zhang et al. (2022) is to take measurements of traits (here, hyphal
C:N:P stoichiometry) at the community level directly.
Does the species × traits become dispensable in mycorrhizal ecology?
Certainly not. Bringing mycorrhizal fungi into cultures, identifying
traits likely to represent important trade-offs in fungal resource
management strategies (Chagnon et al., 2013), ensuring reproducible
measurement of such traits and establishing common resources to share
such traits (Kattge et al., 2020; Zanne et al., 2020) remains a priority
of mycorrhizal ecophysiology. Opinions (Chagnon et al., 2013) and
definitions (Chaudhary et al., 2020) will only be useful if followed by
actual work to populate databases currently storing the very fragmentary
data on fungal traits. We cannot leave aside this important work at the
species and individual scales, because evolutionary trade-offs defining
resource management and life history strategies emerge at those very
scales, not at the community level (Grime & Pierce, 2012).
Trait-environment relationships, however, can inform us on the way
environmental pressures may select for particular species
characteristics, and in this regard, progress can be made over much
shorter timescales than the work expected to rely on permanent culture
banks and individual-level trait measurements. Zhang et al. (2022), for
example, identified an increase in hyphal P concentrations in response
to warming and drought treatments, illustrating hyphal stoichiometry as
a potentially important “response trait” for mycorrhizal fungi. The
upcoming challenge with stoichiometry is now to link form and function.
What is the purpose of enhanced mycelial P for the fungus? Luxury uptake
and storage as polyphosphates, which may confer bargaining power to the
fungus? Increased cellular concentration of “growth-related molecules”
(sensu Zhang et al., 2022) such as RNA? This remains to be
elucidated. The same is true for nitrogen, which can be present in both
growth- and function-related proteins, or in cell wall components
slowing down necromass decomposition (Fernandez et al., 2019). This will
influence how likely are fungal hyphae to contribute to soil organic
pools of different turnover times (See et al., 2022; Klink et al.,
2022).
We can probably identify many other traits that we expect to be (1)
measurable at the community level and (2) associated with environmental
filters. Spore size and wall ornamentations could be linked to dispersal
dynamics (e.g., Chaudhary et al., 2020). Cell wall thickness could be
linked with susceptibility to fungivory (as a constitutive structural
defense), and could be expected to be associated with predation risk,
but also community-level productivity. Generally, structural defenses
are expected to be maximal under harsh conditions promoting conservative
species with long-lived, constitutively defended tissues (Coley, 1988).
Hyphal allocation allometry to the root vs. the soil habitats already
has received considerable attention (e.g., Maherali & Klironomos,
2007), although the assumption that extensive soil foraging is
associated with more efficient P return to host can be questioned
(Jakobsen et al., 1992). Community-level allometric measurements could
be coupled with soil nutrient availability along natural or experimental
gradients could clarify this issue. Relative mycelial investments in the
soil, however, is a multifaceted trait that bears implication for other
aspects of fungal growth and dispersal, namely the colonization of new
patches (emerging roots), the exposition to parasites/predators, and the
interactions with non-mycorrhizal microorganisms potentially including
hyphosphere mutualists. In other words, soil hyphae are not strictly
foraging units, but may also serve dispersal, chemical warfare and
interkingdom cooperation. This may decrease the probability of finding
clear univariate linkages between hyphal allometry and single
environmental filters such as nutrient availability. Other traits
requiring our attention are biomass growth and turnover rates. Tissue
maximal growth rate and lifespan are central to the definition of
ecological strategies (e.g., Westoby et al., 2002; Darling et al.,
2012). In principle, this can be measured at the community level for
mycorrhizal fungi, although the experimental approach should be selected
wisely. Traditional approaches to measuring biomass accumulation in
mycorrhizal studies typically rely either on microcosms inoculated with
fungal propagules, or on ingrowth bags. Both these approaches will
select for colonists that can rapidly invade this new empty niche (a
bulk sterile pot/ingrowth bag), thus biasing our estimates of growth
rates in favor of those displayed by ruderal colonists (i.e.,
community-level trait not matching the community composition/structure).
However, regarding biomass turnover rates, it could be envisaged to
derive such estimate using stable isotope probing targeting a specific
biomarker (e.g., NLFA 16:1ω5). The only drawback is that evaluating
dilution rate of heavy carbon in such a biomarker rapidly makes the cost
per sample prohibitive, hampering measurements of biomass turnover rates
along environmental gradients, or in response to an experimental
treatment.
Despite the technical difficulties associated with measuring
community-level traits, or the challenges to linking form and function,
the approach put forth by Zhang et al. (2022) with hyphal stoichiometry
are part of the equation to advance mycorrhizal ecophysiology, and
should be extended to other traits. Meanwhile, the long-term objective
for mycorrhizal ecophysiologists should still be to isolate and culture
strains, and make these permanent resources for them and other
research groups to measure traits in future studies. Intraspecific trait
variation appears so important, at least for arbuscular mycorrhizal
fungi (e.g., Munkvold et al., 2004; Antunes et al., 2011), that strain
identity will be just as important as species identity in building trait
databases. And as mycorrhizal ecophysiology matures, new traits will
gain interest and have to be measured on those strains for which we have
already measured a number of other traits. Plant and animal
ecophysiologists have a permanent resource they can sample individuals
from: it is called nature. Mycorrhizal ecologists are in need for such
analogous resource: permanent culture banks. Thus, it seems that
challenges lying ahead in mycorrhizal ecophysiology are multifaceted,
encompassing the need for conceptual development, standard laboratory
methods, but also creativity in getting long-term funding to maintain
biological material.