Variability of rRNA Operon Copy Number and Growth Rate Dynamics of Bacillus Isolated from an Extremely Oligotrophic Aquatic Ecosystem

Valdivia-Anistro, Jorge; Eguiarte-Fruns, Luis Enrique; Delgado, Gabriela; Márquez-Zacarías, Pedro; Gasca-Pineda, Jaime; Learned, Jennifer; Elser, James J.; Olmedo-Álvarez, Gabriela; Souza, Valeria

doi:10.3389/fmicb.2015.01486

Cited by 37 publications

(31 citation statements)

References 91 publications

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“…Since we found a similar pattern of CUE increasing with growth rate and rrN even for nonfermentable substrates, this indicates that overflow metabolism was not a uniform driver of CUE and yield at high growth rates in our environmental isolates. This is also consistent with other studies which used aquatic isolates: maximum growth rate and yield were negatively correlated only for a subset of Proteobacteria in one study (32) and were positively correlated for Bacillus species in another (52). Mechanistically, it would make sense that CUE increases with growth rate if (time-dependent) maintenance respiration outstripped (time-independent) growth respiration (13), but neither the literature (54) nor the values derived from the current data set indicate this to be the case.…”

Section: Discussionsupporting

confidence: 92%

Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria

Pold

Domeignoz‐Horta

Morrison

et al. 2020

mBio

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The strategy that microbial decomposers take with respect to using substrate for growth versus maintenance is one essential biological determinant of the propensity of carbon to remain in soil. To quantify the environmental sensitivity of this key physiological trade-off, we characterized the carbon use efficiency (CUE) of 23 soil bacterial isolates across seven phyla at three temperatures and with up to four substrates. Temperature altered CUE in both an isolate-specific manner and a substrate-specific manner. We searched for genes correlated with the temperature sensitivity of CUE on glucose and deemed those functional genes which were similarly correlated with CUE on other substrates to be validated as markers of CUE. Ultimately, we did not identify any such robust functional gene markers of CUE or its temperature sensitivity. However, we found a positive correlation between rRNA operon copy number and CUE, opposite what was expected. We also found that inefficient taxa increased their CUE with temperature, while those with high CUE showed a decrease in CUE with temperature. Together, our results indicate that CUE is a flexible parameter within bacterial taxa and that the temperature sensitivity of CUE is better explained by observed physiology than by genomic composition across diverse taxa. We conclude that the bacterial CUE response to temperature and substrate is more variable than previously thought. IMPORTANCE Soil microbes respond to environmental change by altering how they allocate carbon to growth versus respiration—or carbon use efficiency (CUE). Ecosystem and Earth System models, used to project how global soil C stocks will continue to respond to the climate crisis, often assume that microbes respond homogeneously to changes in the environment. In this study, we quantified how CUE varies with changes in temperature and substrate quality in soil bacteria and evaluated why CUE characteristics may differ between bacterial isolates and in response to altered growth conditions. We found that bacterial taxa capable of rapid growth were more efficient than those limited to slow growth and that taxa with high CUE were more likely to become less efficient at higher temperatures than those that were less efficient to begin with. Together, our results support the idea that the CUE temperature response is constrained by both growth rate and CUE and that this partly explains how bacteria acclimate to a warming world.

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Section: Discussionsupporting

confidence: 92%

Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria

Pold

Domeignoz‐Horta

Morrison

et al. 2020

mBio

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“…Reduced growth after labile C addition could reflect an oligotrophic ecological strategy, as low-resource-adapted organisms are expected to be outcompeted by copiotrophs in nutrient-rich environments (Fierer et al, 2007). This could underlie the reduced growth of Firmicutes observed in this experiment; these taxa were primarily within the class Bacilli, a diverse group containing both relatively copiotrophic and oligotrophic 'species' (Moreno-Letelier et al, 2011;Valvidia-Anistro et al, 2015). Within Bacilli, these growth strategies have been found to sort by phylogeny in cultured representatives (Mitsui et al, 2007).…”

Section: Resultsmentioning

confidence: 81%

Bacterial carbon use plasticity, phylogenetic diversity and the priming of soil organic matter

et al. 2017

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Microorganisms perform most decomposition on Earth, mediating carbon (C) loss from ecosystems, and thereby influencing climate. Yet, how variation in the identity and composition of microbial communities influences ecosystem C balance is far from clear. Using quantitative stable isotope probing of DNA, we show how individual bacterial taxa influence soil C cycling following the addition of labile C (glucose). Specifically, we show that increased decomposition of soil C in response to added glucose (positive priming) occurs as a phylogenetically diverse group of taxa, accounting for a large proportion of the bacterial community, shift toward additional soil C use for growth. Our findings suggest that many microbial taxa exhibit C use plasticity, as most taxa altered their use of glucose and soil organic matter depending upon environmental conditions. In contrast, bacteria that exhibit other responses to glucose (reduced growth or reliance on glucose for additional growth) clustered strongly by phylogeny. These results suggest that positive priming is likely the prototypical response of bacteria to sustained labile C addition, consistent with the widespread occurrence of the positive priming effect in nature.

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“…Adaptive duplications could also be selected for fast growth in nutrient-rich environments. An example could be the occurrence of multiple rrn operons in many microbial species that may be a selected genetic mechanism contributing to fast growth [37][38][39][40][41]. Also, the frequently observed duplication of the tuf gene, encoding elongation factor EF-Tu, may have been selected in different bacterial species because this duplication helps support faster growth rates than are supported by a single gene copy [42][43][44].…”

Section: The Snap Hypothesismentioning

confidence: 99%

The SNAP hypothesis: Chromosomal rearrangements could emerge from positive Selection during Niche Adaptation

Brandis

Hughes

2020

PLoS Genet

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The relative linear order of most genes on bacterial chromosomes is not conserved over evolutionary timescales. One explanation is that selection is weak, allowing recombination to randomize gene order by genetic drift. However, most chromosomal rearrangements are deleterious to fitness. In contrast, we propose the hypothesis that rearrangements in gene order are more likely the result of selection during niche adaptation (SNAP). Partial chromosomal duplications occur very frequently by recombination between direct repeat sequences. Duplicated regions may contain tens to hundreds of genes and segregate quickly unless maintained by selection. Bacteria exposed to non-lethal selections (for example, a requirement to grow on a poor nutrient) can adapt by maintaining a duplication that includes a gene that improves relative fitness. Further improvements in fitness result from the loss or inactivation of non-selected genes within each copy of the duplication. When genes that are essential in single copy are lost from different copies of the duplication, segregation is prevented even if the original selection is lifted. Functional gene loss continues until a new genetic equilibrium is reached. The outcome is a rearranged gene order. Mathematical modelling shows that this process of positive selection to adapt to a new niche can rapidly drive rearrangements in gene order to fixation. Signature features (duplication formation and divergence) of the SNAP model were identified in natural isolates from multiple species showing that the initial two steps in the SNAP process can occur with a remarkably high frequency. Further bioinformatic and experimental analyses are required to test if and to which extend the SNAP process acts on bacterial genomes. Author summaryAll life on earth has evolved from a universal common ancestor with a specific order of genes on the chromosome. This order is not maintained in modern species and the standard hypothesis is that changes reflect a lack of strong selection on gene order. Here, we propose an alternative hypothesis, SNAP. The occupation of a novel environment by bacteria is generally a trade-off situation. For example, while the bacteria may not be adapted PLOS Genetics | https://doi.org/10.1371/journal.pgen.

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Variability of rRNA Operon Copy Number and Growth Rate Dynamics of Bacillus Isolated from an Extremely Oligotrophic Aquatic Ecosystem

Cited by 37 publications

References 91 publications

Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria

Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria

Bacterial carbon use plasticity, phylogenetic diversity and the priming of soil organic matter

The SNAP hypothesis: Chromosomal rearrangements could emerge from positive Selection during Niche Adaptation

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