Interactions between environmental factors shape the fitness and
traits of individual microorganisms
Environmental factors often combine non additively to shape the
phenotypes and fitness of microorganisms
(Kaplan et al., 2008;
Okano et al., 2020; Wood et al., 2012). Interactions between
environmental factors on microbial growth and phenotypes have been a
major focus of microbiology since the early days of the discipline
(Blaiseau and Holmes,
2021). Among the most iconic examples we find diauxic growth, whereby
microorganisms consume nutrients in succession, rather than
simultaneously. The effect of a nutrient on the growth of a
microorganism will thus be masked by the presence of another nutrient
whose hierarchy in the diauxic choice is higher
(Aidelberg et al.,
2014; Bajic and Sanchez, 2020). This interaction between nutrients is
akin to the phenomenon of dominance in genetics, an interaction whose
result is the masking of the phenotypic effect of an allele by the
presence of another (dominant) allele in a diploid organism.
Diauxic growth is implemented by genetic networks that respond to the
presence of more than one input nutrient by activating the metabolic
pathways required to metabolize just one of them, but not the others.
Beyond the specific example of diauxie, many microbial gene-regulatory
networks integrate multiple environmental inputs
(Espinar et al., 2013;
Kaplan et al., 2008), and bacterial promoters commonly contain binding
sites for multiple different transcription factors
(Bintu et al., 2005;
Rydenfelt et al., 2014). The combinatorial nature of gene regulatory
networks and their ability to integrate multiple environmental signals
provides a basis for the emergence of complex interactions between
environmental factors.
Interactions between environmental factors do not need to have a gene
regulatory basis. An example are the well-characterized interactions
between antibiotics. It has been shown that antibiotics targeting
different cellular processes often act synergistically
(Cacace et al., 2023;
Yeh et al., 2006), whereby the detrimental effect of an antibiotic is
higher than expected when a second antibiotic is present too
(Yeh et al., 2009).
Systematic screens of interactions between antibiotics have found that
they are pervasive in both Gram positive and Gram negative bacterial
species (Wood et al.,
2012), and they can exhibit substantial complexity
(Lázár et al., 2022).
Antibiotics can also interact with physical environmental factors, and
their very presence in the medium can alter the optimal growth
temperature of bacteria, and modulate the effect of stressful
temperatures
(Cruz-Loya et al.,
2021). The idea that two or more stressors may act non-additively is an
old concept in microbial ecology (for a recent example see
(Smith et al.,
2023)), which in fact extends well beyond the realm of microorganisms
(Côté et al., 2016).
Interactions between environmental factors may affect biotechnologically
significant traits. For instance, Skonieczny & Yargeau examined the
combined effect of the initial pH and initial glucose concentration on
the rate of H2 produced by populations of the bacteriumClostridium beijerinckii(Skonieczny and
Yargeau, 2009). At low initial glucose concentrations,
H2 production peaked at pH=6.1. Yet, when higher initial
concentrations of glucose were provided, the peak shifted to higher
values of pH, close to 6.5. In other words, an increase in glucose
concentration changes the response of H2 production to
pH, and this affects the optimal pH in the culture. This particular case
exemplifies the potential significance of interactions between
environmental factors in biotechnology, and we did not have to dig
deeply to find it. Most environmental factors exhibit a non-additive
effect even when they are the only ones being changed. Take for instance
the example of Temperature. Microbial Temperature response curves are
not only non-linear but also non-monotonic. A 2oC
increase in Temperature will have a positive effect in the carbon use
efficiency of microorganisms below their optimal temperature
(Smith et al., 2021),
but a detrimental effect when it takes place above that point. This
well-known example illustrates the many challenges of predicting the
effect of the environment on organismal traits, a challenge that extends
to the community level.