Microorganisms commonly inhabit energy-limited ecosystems where cellular maintenance and reproduction is highly constrained. To gain insight into how individuals persist under such conditions, we derived demographic parameters from a collection of 21 heterotrophic bacterial taxa by censusing 100 populations in an effectively closed system for 1,000 d. All but one taxon survived prolonged resource scarcity, yielding estimated times to extinction ranging over four orders of magnitude from 10 0 to 10 5 y. Our findings corroborate reports of long-lived bacteria recovered from ancient environmental samples, while providing insight into mechanisms of persistence. As death rates declined over time, lifespan was extended through the scavenging of dead cells. Although reproduction was suppressed in the absence of exogenous resources, populations continued to evolve. Hundreds of mutations were acquired, contributing to genome-wide signatures of purifying selection as well as molecular signals of adaptation. Consistent ecological and evolutionary dynamics indicate that distantly related bacteria respond to energy limitation in a similar and predictable manner, which likely contributes to the stability and robustness of microbial life.
more »
« less
Molecular Evolutionary Dynamics of Energy Limited Microorganisms
Abstract Microorganisms have the unique ability to survive extended periods of time in environments with extremely low levels of exploitable energy. To determine the extent that energy limitation affects microbial evolution, we examined the molecular evolutionary dynamics of a phylogenetically diverse set of taxa over the course of 1,000 days. We found that periodic exposure to energy limitation affected the rate of molecular evolution, the accumulation of genetic diversity, and the rate of extinction. We then determined the degree that energy limitation affected the spectrum of mutations as well as the direction of evolution at the gene level. Our results suggest that the initial depletion of energy altered the direction and rate of molecular evolution within each taxon, though after the initial depletion the rate and direction did not substantially change. However, this consistent pattern became diminished when comparisons were performed across phylogenetically distant taxa, suggesting that although the dynamics of molecular evolution under energy limitation are highly generalizable across the microbial tree of life, the targets of adaptation are specific to a given taxon.
more »
« less
- Award ID(s):
- 1934554
- PAR ID:
- 10313289
- Editor(s):
- Battistuzzi, Fabia Ursula
- Date Published:
- Journal Name:
- Molecular Biology and Evolution
- Volume:
- 38
- Issue:
- 10
- ISSN:
- 1537-1719
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Antagonistic interactions are widespread in the microbial world and affect microbial evolutionary dynamics. Natural microbial communities often display spatial structure, which affects biological interactions, but much of what we know about microbial antagonism comes from laboratory studies of well-mixed communities. To overcome this limitation, we manipulated two killer strains of the budding yeastSaccharomyces cerevisiae, expressing different toxins, to independently control the rate at which they released their toxins. We developed mathematical models that predict the experimental dynamics of competition between toxin-producing strains in both well-mixed and spatially structured populations. In both situations, we experimentally verified theory’s prediction that a stronger antagonist can invade a weaker one only if the initial invading population exceeds a critical frequency or size. Finally, we found that toxin-resistant cells and weaker killers arose in spatially structured competitions between toxin-producing strains, suggesting that adaptive evolution can affect the outcome of microbial antagonism in spatial settings.more » « less
-
Abstract Wetland and permafrost soils contain some of Earth's largest reservoirs of organic carbon, and these stores are threatened by rapid warming across the Arctic. Nearly half of northern wetlands are affected by permafrost. As these ecosystems warm, the cycling of dissolved organic matter (DOM) and the opportunities for microbial degradation are changing. This is particularly evident as the relationship between wetland and permafrost DOM dynamics evolves, especially with the introduction of permafrost‐derived DOM into wetland environments. Thus, understanding the interplay of DOM composition and microbial communities from wetlands and permafrost is critical to predicting the impact of released carbon on global carbon cycling. As little is understood about the interactions between wetland active layer and permafrost‐derived sources as they intermingle, we conducted experimental bioincubations of mixtures of DOM and microbial communities from two fen wetland depths (shallow: 0–15 cm, and deep: 15–30 cm) and two ages of permafrost soil (Holocene and Pleistocene). We found that the source of microbial inoculum was not a significant driver of dissolved organic carbon (DOC) degradation across treatments; rather, DOM source and specifically, DOM molecular composition, controlled the rate of DOC loss over 100 days of bioincubations. DOC loss across all treatments was negatively correlated with modified aromaticity index, O/C, and the relative abundance of condensed aromatic and polyphenolic formula, and positively correlated with H/C and the relative abundance of aliphatic and peptide‐like formula. Pleistocene permafrost‐derived DOC exhibited ∼70% loss during the bioincubation driven by its initial molecular‐level composition, highlighting its high bioavailability irrespective of microbial source.more » « less
-
Previously, the authors published a framework for phylogenetically informed reconstruction of appendicular musculature in extinct synapsids. In the present study, this framework is employed to rigorously infer the arrangement of muscles in the hindlimb of eight exemplar taxa that capture the evolutionary transformation from basal synapsids to crown therians. Muscle maps detailing origins and insertions are presented for each taxon. These will aid the interpretation of fossil material in the future, especially fragmentary remains of related species, and provide a foundation for functional analysis of the appendicular skeleton and its evolution.more » « less
-
The putative Hispaniolan endemic Graffenrieda ottoschulzii (syn. = Miconia ottoschulzii) was evaluated morphologically and phylogenetically. Morphological data clearly place the species within Miconia, as the taxon is missing the dorsal appendage on the connective and capsule fruits of Graffenrieda but has the berry fruits of Miconia. Phylogenetically G. ottoschulzii was resolved as sister to the widespread and mostly South American, M. pyrifolia, and we conclude here that the two taxa are conspecific. We provide an updated description of M. pyrifolia and lectotypify the names M. ottoschulzii and M. pyrifolia.more » « less
An official website of the United States government

