Warmer and drier ecosystems select for smaller bacterial genomes in global soils
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2770596x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/imt2.70 by Readcube (Labtiva Inc.), Wiley Online Library on [12/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Received: 4 September 2022 | Revised: 1 November 2022 | Accepted: 28 November 2022
DOI: 10.1002/imt2.70
SHORT COMMUNICATION
Warmer and drier ecosystems select for smaller bacterial
genomes in global soils
Hongwei Liu1 | Haiyang Zhang1,2 | Jeff Powell1 |
Manuel Delgado‐Baquerizo3,4 | Juntao Wang1,5 | Brajesh Singh1,5
1
Hawkesbury Institute for the
Environment, Western Sydney Abstract
University, Penrith, New South Wales, Bacterial genome size reflects bacterial evolutionary processes and metabolic
Australia
2
lifestyles, with implications for microbial community assembly and ecosystem
College of Life Sciences, Hebei
University, Baoding, China functions. However, to understand the extent of genome‐mediated microbial
3
Laboratorio de Biodiversidad y responses to environmental selections, we require studies that observe genome
Funcionamiento Ecosistemico, Instituto size distributions along environmental gradients representing different
de Recursos Naturales y Agrobiología de
conditions that soil bacteria normally encounter. In this study, we used
Sevilla (IRNAS), CSIC, Sevilla, Spain
4
Unidad Asociada CSIC‐UPO (BioFun),
surface soils collected from 237 sites across the globe and analyzed how
Universidad Pablo de Olavide, Sevilla, environmental conditions (e.g., soil carbon and nutrients, aridity, pH, and
Spain temperature) affect soil bacterial occurrences and genome size at the
5
Global Centre for Land‐Based
community level using bacterial community profiling. We used a joint species
Innovation, Western Sydney University,
Penrith, New South Wales, Australia distribution model to quantify the effects of environments on species
occurrences and found that aridity was a major regulator of genome size
Correspondence
with warmer and drier environments selecting bacteria with smaller genomes.
Haiyang Zhang, Hawkesbury Institute for
the Environment, Western Sydney Drought‐induced physiological constraints on bacterial growth (e.g., water
University, Penrith, NSW 2753, Australia. scarcity for cell metabolisms) may have led to these correlations. This finding
Email: haiyang.zhang@westernsydney.
edu.au
suggests that increasing cover by warmer and drier ecosystems may result in
bacterial genome simplifications by a reduction of genome size.
KEYWORDS
aridity, climate impacts, genome size, global soil, microbial trait, soil nutrients
Highlights
• A joint species distribution model was used to quantify the environmental
effects on occurrences of bacterial species.
• Warmer and drier environments favored bacteria with smaller genomes.
• Higher soil fertility (e.g., phosphorous) favored bacteria with smaller
genomes.
Hongwei Liu and Haiyang Zhang contributed equally to this study.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided
the original work is properly cited.
© 2023 The Authors. iMeta published by John Wiley & Sons Australia, Ltd on behalf of iMeta Science.
iMeta. 2023;e70. wileyonlinelibrary.com/journal/imeta | 1 of 7
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2 of 7 | LIU ET AL.
Trait‐based approaches have revolutionized ecology and one‐end of the gradients) can exist in scaled‐up/global
provided demonstrable value to our ecological under- scale environmental investigations [15]. Such environ-
standing (e.g., community assembly) of many taxa. mental effects on microbial species occurrences can be
However, knowledge of the importance of microbial either positive, negative, or neutral (Figure 1A), and the
traits lags behind other organisms (e.g., plants). In magnitude of the effect differs among bacterial species.
particular, we know little about the biogeographic To this end, four types of relationships between
pattern of microbial traits across the globe and the extent environmental effects and bacterial genome size are
to which they are under environmental selection [1, 2]. proposed: (i) trade‐offs (Figure 1B), (ii)–(iii) uni-
Among microbial traits, genome size is fundamental for directional effects (Figure 1C,D), and (iv) no correlations
the prediction of microbial physiology, their ecological (Figure 1E). In this study, we aimed to investigate
relationships with other microbes and the environment, whether genome size could mediate the effects of
and their evolutionary histories. This is because (i) environmental gradients on bacterial occurrences at the
genome size is linked to other bacterial traits related to global scale. We hypothesized that environments with
life history strategies, for example, growth rate and less favorable conditions such as drier soils (Figure 1F),
tolerance to extreme conditions [3, 4], (ii) variation in warmer climates (Figure 1G), and reduced availability of
genome size among microbial taxa can reflect evolu- soil nutrients (Figure 1H) favor occurrences of bacterial
tionary events such as genome expansion and reduction species with smaller genomes. These hypotheses are
that may be associated with emerging of new species, based on the large genome constraint hypothesis [6], and
functions or lifestyles [5, 6], and (iii) organisms with previous findings that nutrient limitation/drought‐
large genomes require more resources to grow and induced physiological constraints on growth (e.g., water
reproduce and can have a more restricted ecological scarcity for cell metabolisms) may lead to genome
distribution (large genome constraint hypothesis) [7]. In streamlining (e.g., gene loss) [18].
other words, smaller bacterial genomes require lower To test the above hypotheses, we analyzed bacterial
numbers of AGCT, and they can be more advantageous communities of soil samples collected from 237 locations
in nutrient‐limited (e.g., nitrogen, N and phosphorus, P) across the globe (Supporting Information: Figure S1),
environments [7]. Therefore, the distribution of genomic covering different ecosystem types (forests, grasslands, and
traits in environments may exhibit unique patterns shrublands) and diverse environmental gradients such as soil
reflecting nutrient conditions. aridity, nutrients, and air temperature [19]. The soil
Soil is a complex and heterogeneous ecosystem, and properties showed a wide range of variations, with soil pH
involves dynamic interactive bacterial communities that ranging from 4.04 to 9.21, soil C ranging from 0.15% to
play key roles in regulating terrestrial nutrient cycling 34.77%, soil N ranging from 0.02% to 1.57%, soil P ranging
and plant productivity. Its function is strictly dependent from 75.10 to 4111.04 mg P kg−1 soil. These sites spanned a
on critical factors like water, light, and biodiversity, gradient of −11.4°C to 26.5°C mean annual temperature and
which provide the sustenance of humanity [8]. Recent 67–3085 mm mean annual precipitation. In total 135,175 soil
studies have investigated microbial genome size in bacterial features (2315 genera, sequence variants analyzed
response to ecosystem type, trophic strategy, and oxygen by QIIME2 software, http://qiime2.org/) were detected using
use [9, 10], but investigations in soil microbial genomes 16S ribosomal RNA (rRNA) gene amplicon sequencing, and
and their responses to environmental factors along large bacterial features annotated at the genus level were extracted
spatial gradients are still limited. Current uncertainties in (see Supporting Information methods, Figures S2, S3, and
the biogeography of soil microbial genome size are due to S4). Those unidentified and less identified bacterial genera,
two main reasons. First, investigations often focus on the such as bacterium culture clones were removed from the
relationship between a single environmental factor and genera feature table. To evaluate whether aggregation of
genome size, yet to identify the most important environ- these data at the genus level was appropriate, we surveyed
mental factors requires multifactorial investigation. For bacterial genome size in the bacteria trait database [20],
example, recent studies only investigated microbial where data for both culturable and unculturable bacterial
genome size interactions with the environment in species are included for these genera. We found that across
response to warming [11–13] and nutrient availability the species within most (95%) bacterial genera (n = 2238)
[14]. Second, these studies investigated only a narrow had a low coefficient of variation (CV) (2770596x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/imt2.70 by Readcube (Labtiva Inc.), Wiley Online Library on [12/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
GLOBAL SOIL BACTERIAL ASSEMBLY ALONG ENVIRONMENTAL GRADIENTS | 3 of 7
(B) (C)
(A)
(D) (E)
(F) (G) (H)
(I)
F I G U R E 1 Conception and hypotheses. The ecological responses of the probabilities of bacterial occurrences to environmental
gradients: positive (yellow), negative (black), and neutral (gray) (A). A positive (or negative) effect size indicates bacteria tend to occur with
higher (or lower) probability when specific environmental conditions increase. An effect size is the slope of the relationship between
bacterial occurrence probability and environmental conditions, calculated by beta parameters from a joint species distribution model
[16, 17]. We provide four types of correlations between microbial traits and the effects size of environments. These are (i) trade‐offs where
trait effects are bidirectional: the effect of the environmental gradients on the probability of species occurrence positively (red) or negatively
(blue) shifts along the trait gradient (B), (ii) and (iii) the trait only exhibits an effect at one end of the environmental gradient, with only a
unidirectional effect when trait values are low (C) or high (D); and (iv) no environmental effects across all trait levels (E). We hypothesized
that shifting from favorable soil conditions to stressful environments (i.e., warmer and drier climates) favors bacteria with small GS in soil.
In detail, we hypothesized that nutrients (carbon, nitrogen, and phosphorous) are positively associated with bacterial genome sizes (F),
while maximum annual temperature (MAXT) (G) and aridity (H) are negatively associated with bacterial genome sizes. Overall, we
hypothesized that stress conditions select bacteria with small genome sizes (I).
sensitivity analysis, details in Supporting Information: We then investigated relationships between the environ-
Figure S3). Thus, we set a CV threshold of 11% across mental gradients and bacterial genome size by fitting the
observations within a genus to select bacterial genera for data set with a joint species distribution model‐hierarchical
inclusion in subsequent analyses, with 1237 bacterial genera modeling of species communities (HMSC) [16, 17] (Support-
being retained. We then matched our global soil microbiome ing Information: Figure S6). After model fitting and
data with these bacterial genera [20], resulting in 143 evaluation, we extracted the effect size, that is, the slope of
bacterial genera with genome size values, ranging from the relationship between bacteria occurrence probability and
1.58 Mbp (Rickettsiella) to 16.04 Mbp (Minicystis) (Supporting environmental conditions, which was the beta‐parameters
Information: Figure S4). Our selected genera included both from HMSC with at least 95% posterior probability. For the
abundant and rare genera (Supporting Information: correlation between genome size and the magnitude of
Figure S5). environmental effects on bacterial occurrence probability, we2770596x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/imt2.70 by Readcube (Labtiva Inc.), Wiley Online Library on [12/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
4 of 7 | LIU ET AL.
(A) (B) (C)
(D) (E) (F)
F I G U R E 2 Correlations between bacterial genome size (log‐transformed; Mbp) and the effects of environmental conditions on bacterial
occurrence. Y axis indicates effect sizes of an environmental condition, which are slopes (beta‐parameters) of the relationship between
bacterial occurrence probability and environmental conditions, calculated from the Hierarchical Modeling of Species Communities (HMSC).
A positive (or negative) effect size indicates bacterial genera tend to occur with higher (or lower) probability when specific environmental
conditions increase. Solid blue lines indicate correlations being significant (p < 0.05) and were fitted considering phylogenetic correlations
among bacteria genera. Aridity index reflects soil water availability (i.e., mean annual precipitation/evapotranspiration). MAXT, mean max
annual temperature.
performed phylogenetic least squares regression to account in arid ecosystem may result in bacterial genome
for phylogenetic autocorrelation among genera given that simplification. Consistently, a recent study also reported a
bacterial genome size is linked with their evolutionary positive correlation between bacterial community weight
history [21]. We found that the distance from the equator mean genome size with mean annual precipitation [23].
(absolute latitude) had a strong impact on genome size However, it is unclear in their study whether the positive
distribution in the soil (Figure 2A, R2 = 0.22, p < 0.00001), in correlation was caused by the bacteria with large genome
that bacteria with small genomes were more likely to have a sizes being positively selected by increasing water availa-
positive association with increasing latitude while bacteria bility or bacteria with small genome sizes being excluded
with large genomes exhibited the opposite. This result was in by increasing water availability, or both. Our results
line with the geographical patterns previously reported [22], support the second scenario, where bacterial species with
where the average‐genome size of bacterial communities small genome sizes had more negative responses to
decreased as distance from the equator increased. increased water availability than those with large genome
Importantly, we found that bacterial genome size size species. Similarly, warmer climates, as indicated by
significantly correlated with aridity (Figure 2B, R2 = 0.27, higher mean maximum temperature (MAXT), favored the
p < 0.00001), in that bacteria with small genomes exhibited occurrence of bacteria with small genome size by excluding
positive responses to increasing aridity (negative response large genome‐sized bacteria (Figure 2C, R2 = 0.06,
to an increasing aridity index) while bacterial genera with p = 0.003). This result is consistent with findings in
large genomes tended to not exhibit any response to aridity previous reports [12, 24], and supported by our further
(the effect sizes related these bacteria were close to zero) analyses, which showed large genome‐sized bacterial
(Figure 2B). This trend of bacterial selection with small species had a lower optimum temperature (Supporting
genomes was consistent across different taxonomic levels Information: Figure S8B, R2 = 0.07, p = 0.001). This means
such as the order and phylum level (Supporting Informa- that an increased temperature can induce higher selective
tion: Figure S7). Our further analyses demonstrated that pressures on bacteria with large genome sizes than on
large genome‐sized bacterial species contain a larger bacteria with small genome sizes.
number of genes (Supporting Information: Figure S6A, We also found that bacterial genome sizes weakly but
R2 = 0.97, p < 0.00001) (Supporting Information: significantly correlated with soil carbon (C, Figure 2D,
Figure S8A), which suggests that a genome size reduction R2 = 0.07, p = 0.001) and P (Figure 2E, R2 = 0.02,2770596x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/imt2.70 by Readcube (Labtiva Inc.), Wiley Online Library on [12/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
GLOBAL SOIL BACTERIAL ASSEMBLY ALONG ENVIRONMENTAL GRADIENTS | 5 of 7
p = 0.035) concentrations, in that bacteria with small (Supporting Information: Figure S10), which may high-
genomes exhibited less negative responses to increasing light the strength of the joint species distribution
soil C or more positive responses to increasing soil P, approach in detecting soil bacterial responses to envir-
suggesting that higher soil fertility favors bacteria with onmental changes. Recent studies indicated that the
smaller genomes. Soil nitrogen did not exhibit a model‐based approach outperforms the CWM‐based
significant correlation (Figure 2F). While contradicting approaches in terms of results accuracy and statistical
our hypothesis (based on the large genome constraint power [28, 29].
theory), our results are supported by previous studies Overall, our study provides novel evidence that
where enrichments of soil nutrients (e.g., P) decreased environmental stress associated with increases in
the mean genome sizes of bacteria at the community aridity and warmer climates favors bacteria with
level in grassland soil [14]. These findings suggest that smaller genomes in soils. Drought‐induced physiolog-
larger genome‐sized bacterial species can dominate in ical constraints on growth (e.g., water scarcity for cell
environments where resources are scarce but diverse, metabolisms) may have led to these correlations.
and where there is little penalty for slow‐growth soil Bacterial community change can lead to changes in
bacteria, in terms of their colonization and competition soil ecological processes such as carbon sequestration.
in soils [22, 25]. It would be also important to investigate For example, previous studies showed that bacteria
how genome size responses to soil nutrient availability with small genomes are associated with high carbon
are linked with their r/K strategy in future studies. For use efficiency (CUE, i.e., the ratio of net carbon gain
example, previous studies showed that soil bacteria from to gross carbon assimilation, a key factor that controls
copiotrophic (r strategy) Firmicutes increased in relative carbon sequestration) [30]. Drought stress reduces
abundance by nutrient addition while oligotrophic (K plant carbon assimilation and availability to soil
strategy) bacteria such as Actinobacteria decreased in microbes. Shifting to a small genome‐size‐dominated
abundance [26]. Consistently, we found that Firmicutes community is important to increase CUE at the
had relatively small and Actinobacteria had large community level and help the ecosystem to maintain
genomes (Supporting Information: Figure S5), and, functions under stressful conditions. Favoring bacte-
therefore, our results (higher soil fertility favors bacteria rial species with small genome sizes may also have
with small genomes) can be explained by the r/K consequences on the redundancy of microbial func-
selection theory [27]. We also found that genome size tions and resilience. Soil microbes make up a complex
did not affect the sensitivity of bacterial occurrence gene pool; reducing or discarding genes for redundant
probability to changes in soil pH and mean minimum metabolic burdens may be a strategy for microbes to
annual temperature (Supporting Information: Figure S9). survive stresses [13]. Now we are facing climate
By contrast, bacterial genome size significantly correlated change that is more rapid than ever before. Despite
with net primary production (NPP, the carbon amount the unknown consequences of such microbial changes
retained by plants or other primary producers) and to ecosystem functions, future climate change
ultraviolet (UV) light, in that bacteria with large genomes research and policy‐making should consider soil
exhibited positive correlations to increasing NPP and UV bacteria and their functional traits as they play
light while bacterial genera with small genomes tended important roles in soil carbon sequestration and
to not exhibit any correlations with NPP and UV light maintaining ecosystem functions. Our study also
(Supporting Information: Figure S9). Increasing NPP suggests that lower soil fertility (soil C and P) and
favored bacteria with large genomes was in line with our higher UV light levels favor bacteria with larger
results that warming and drier ecosystems selected for genomes, which can dominate in soils where
smaller bacterial genomes, because NPP is generally resources are scarce but without major restrictions
lower under stressed environments (e.g., drought). A on slow‐growing bacteria. These findings point
positive response to UV light intensity also indicates that toward fundamental mechanisms underpinning
large genome‐sized bacteria are more tolerant to strong nucleotide selection in bacterial communities in
UV light. Mechanisms for these findings are still unclear global soils. The knowledge is also critical for efforts
and require future studies to investigate in‐depth. to predict biogeochemical feedback in the future
We acknowledge that the community‐weighted trait climate system, where drought events are expected
means (CWM), which is the average of trait values for to occur more frequently and to last longer at a global
species at each site weighted by species abundance, is scale. Our study employed bacterial analyses at the
also commonly used to study trait–environment relation- genus level by obtaining genome size data from a
ships. However, we did not observe significant patterns publicly available database. This method is reliable
between CWM genome size and environmental gradients in testing our hypothesis, and it provides a useful2770596x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/imt2.70 by Readcube (Labtiva Inc.), Wiley Online Library on [12/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
6 of 7 | LIU ET AL.
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