Interactions between environmental factors shape the composition
and function of microbial communities
Environmental factors often combine non additively to shape the
functions and taxonomic composition of microbial communities and the
traits and phenotypes of microbial populations
(Dal Bello et al.,
2021; Estrela et al., 2021a, 2021b; Fonte et al., 2013; Lázár et al.,
2022; Pacheco et al., 2021; Pacheco and Segrè, 2021; Replansky and Bell,
2009; Smith et al., 2023; Wood et al., 2012). In what follows, we
provide a few recent examples of environmental interactions in the
context of community composition and function, with the aim of
illustrating this point.
Nutrients interact non additively to determine community
composition. Microbial communities assemble in complex environments
that contain multiple resources. These resources can have different
effects in different members of the community: a molecule that is
discarded by a microorganism is often useful for others
(D’Souza et al., 2018;
Goldford et al., 2018; Mataigne et al., 2021). In a recent study
(Estrela et al.,
2021b), we have systematically investigated how nutrients combine to
shape the taxonomic composition of microbial communities. Through an
enrichment approach from soil and plant communities (described in detail
elsewhere (Estrela et
al., 2021a)), we studied the taxonomic composition of stable, serially
passaged communities in media containing various sets of two growth
limiting nutrients, and compared these with the community compositions
that formed in each nutrient separately. We found that interactions
between nutrients were often strong. Increasing the number of supplied
resources from one to two or even three had no effect on the total
diversity of our enrichment communities
(Estrela et al.,
2021a), and this was often due to an effect we termed “nutrient
dominance”, where one of the two nutrients masked the ability of the
other to recruit taxa into the community
(Estrela et al.,
2021b). For example, the taxonomic composition of enrichment
communities where both glycerol and succinate were supplied externally
as the only carbon sources were nearly indistinguishable from the
composition of the communities assembled in glycerol alone. The majority
of the taxa that were coexisting stably when succinate was the only
supplied nutrient were excluded from the community when glycerol was
also supplied in the culture medium at the beginning of every passage
(Estrela et al.,
2021b).
These results echo similar findings from other groups. Pacheco and Segre
(Pacheco et al.,
2021) found strong non-additive interactions between nutrients in
serially passaged, defined communities, and Dal Bello et al
(Dal Bello et al.,
2021) found that community richness increased very weakly as we
increase the number of supplied resources, barely doubling as we went
from 1 to 32. Together with older evidence
(Replansky and Bell,
2009) these studies support the idea that nutrients often interact non
additively in their effect on community composition. It stands to reason
that such non-additivity will extend to function also.
Environmental variables interact non additively to
determine community functions. In addition to their non-additive
effect on the taxonomic composition of a community, the effect of two or
more environmental variables on community functions is also often non
additive. For instance, Jimenez et al studied the combined effect of
different environmental variables on the methanogenic output of an
anaerobic digestor community
(Jiménez et al.,
2014). Specifically, these authors examined the combined effect of
three substrates (pig manure, rice straw and clay residual) at different
concentrations on the specific methanogenic activity of the digester
community, and employed a fractional factorial design followed by a
linear regression with interaction terms to predict out of sample. Their
approach revealed the existence of strong pairwise interactions between
the substrates, particularly for clay residual and rice straw under
mesophilic conditions. The interactions were strong enough to change the
sign effect of increasing clay concentration at high vs low manure
concentrations: increasing clay concentration had a positive effect on
the methanogenic activity when manure concentration was low, but a
negative effect when manure concentration was high. Sign-effect
interactions (akin to sign epistasis in genetics) are common in
microbial consortia
(Sanchez et al.,
2023).
In another study, Molina-Barahona et al sought to optimize the
environmental conditions for diesel removal in contaminated soils
through biostimulation
(Molina-Barahona et
al., 2004). To this end, they investigated the combinatorial effects of
various environmental factors that are known to individually have an
effect on diesel removal rate: C:N ratio, moisture, and the amount and
type of crop residue (CR). These factors were individually toggled
between two values and combinations were generated through a fractional
factorial design approach. The authors then found that interactions
between moisture and CR type had a modest but significant effect on the
amount of diesel removed in microcosms, as the amount of diesel removed
in the presence of both factors at the same time was higher than
expected by the product of each in isolation
(Molina-Barahona et
al., 2004) .
On a similar vein, Zhou et al, studied the combined effect of three
binary variables: glucose addition, sodium dodecyl benzene sulfonate
(SDBS) addition, and immobilization of the bacteria on biochar (or lack
thereof) on the biodegradation of polycyclic aromatic hydrocarbons (PAH)
by a microbial consortium
(Zhou et al., 2023).
While glucose alone stimulated PAH biodegradation, it had a negligible
effect when combined with SDBS unless the consortia was also
immobilized. In this instance, glucose had a modest (but seemingly
significant) positive effect on the degradation of low molecular weight
PAH. The authors propose a mechanistic explanation for this three-way
interaction: Glucose had been previously found to stimulate the
metabolism of PAHs and it is also known to promote microorganism to
absorb more PAHs. In turn, SDBS is believed to increase the
bioavailability of PAHs by enhancing their mobility and bringing them
closer to the immobilized bacteria
(Zhou et al., 2023).
All of these examples illustrate the potential effect of environmental
interactions in the performance of single and multi-strain microbial
consortia. On the one hand, the functional response of microbial
consortia to environmental manipulations creates opportunities for their
optimization. On the other hand, the combinatorial complexity of these
environmental interaction effects may appear to be dissuasive. While it
is indeed undoubtedly challenging, as we will see below there exists
clear and convincing evidence that it is far from impossible.