skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Long-Term m5C Methylome Dynamics Parallel Phenotypic Adaptation in the Cyanobacterium Trichodesmium
Abstract A major challenge in modern biology is understanding how the effects of short-term biological responses influence long-term evolutionary adaptation, defined as a genetically determined increase in fitness to novel environments. This is particularly important in globally important microbes experiencing rapid global change, due to their influence on food webs, biogeochemical cycles, and climate. Epigenetic modifications like methylation have been demonstrated to influence short-term plastic responses, which ultimately impact long-term adaptive responses to environmental change. However, there remains a paucity of empirical research examining long-term methylation dynamics during environmental adaptation in nonmodel, ecologically important microbes. Here, we show the first empirical evidence in a marine prokaryote for long-term m5C methylome modifications correlated with phenotypic adaptation to CO2, using a 7-year evolution experiment (1,000+ generations) with the biogeochemically important marine cyanobacterium Trichodesmium. We identify m5C methylated sites that rapidly changed in response to high (750 µatm) CO2 exposure and were maintained for at least 4.5 years of CO2 selection. After 7 years of CO2 selection, however, m5C methylation levels that initially responded to high-CO2 returned to ancestral, ambient CO2 levels. Concurrently, high-CO2 adapted growth and N2 fixation rates remained significantly higher than those of ambient CO2 adapted cell lines irrespective of CO2 concentration, a trend consistent with genetic assimilation theory. These data demonstrate the maintenance of CO2-responsive m5C methylation for 4.5 years alongside phenotypic adaptation before returning to ancestral methylation levels. These observations in a globally distributed marine prokaryote provide critical evolutionary insights into biogeochemically important traits under global change.  more » « less
Award ID(s):
1657757 1851222 1260490
PAR ID:
10212746
Author(s) / Creator(s):
; ; ; ; ; ;
Date Published:
Journal Name:
Molecular Biology and Evolution
ISSN:
0737-4038
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Adaptive evolution and phenotypic plasticity will fuel resilience in the geologically unprecedented warming and acidification of the earth’s oceans, however, we have much to learn about the interactions and costs of these mechanisms of resilience. Here, using 20 generations of experimental evolution followed by three generations of reciprocal transplants, we investigated the relationship between adaptation and plasticity in the marine copepod,Acartia tonsa, in future global change conditions (high temperature and high CO2). We found parallel adaptation to global change conditions in genes related to stress response, gene expression regulation, actin regulation, developmental processes, and energy production. However, reciprocal transplantation showed that adaptation resulted in a loss of transcriptional plasticity, reduced fecundity, and reduced population growth when global change-adapted animals were returned to ambient conditions or reared in low food conditions. However, after three successive transplant generations, global change-adapted animals were able to match the ambient-adaptive transcriptional profile. Concurrent changes in allele frequencies and erosion of nucleotide diversity suggest that this recovery occurred via adaptation back to ancestral conditions. These results demonstrate that while plasticity facilitated initial survival in global change conditions, it eroded after 20 generations as populations adapted, limiting resilience to new stressors and previously benign environments. 
    more » « less
  2. The role of phenotypic plasticity in adaptive evolution has been debated for decades. This is because the strength of natural selection is dependent on the direction and magnitude of phenotypic responses to environmental signals. Therefore, the connection between plasticity and adaptation will depend on the patterns of plasticity harbored by ancestral populations before a change in the environment. Yet few studies have directly assessed ancestral variation in plasticity and tracked phenotypic changes over time. Here we resurrected historic propagules ofDaphniaspanning multiple species and lakes in Wisconsin following the invasion and proliferation of a novel predator (spiny waterflea,Bythotrephes longimanus). This approach revealed extensive genetic variation in predator-induced plasticity in ancestral populations ofDaphnia. It is unlikely that the standing patterns of plasticity shieldedDaphniafrom selection to permit long-term coexistence with a novel predator. Instead, this variation in plasticity provided the raw materials forBythotrephes-mediated selection to drive rapid shifts inDaphniabehavior and life history. Surprisingly, there was little evidence for the evolution of trait plasticity as genetic variation in plasticity was maintained in the face of a novel predator. Such results provide insight into the link between plasticity and adaptation and highlight the importance of quantifying genetic variation in plasticity when evaluating the drivers of evolutionary change in the wild. 
    more » « less
  3. Tringe, Susannah Green (Ed.)
    ABSTRACT Below-ground carbon transformations that contribute to healthy soils represent a natural climate change mitigation, but newly acquired traits adaptive to climate stress may alter microbial feedback mechanisms. To better define microbial evolutionary responses to long-term climate warming, we study microorganisms from an ongoingin situsoil warming experiment where, for over three decades, temperate forest soils are continuously heated at 5°C above ambient. We hypothesize that across generations of chronic warming, genomic signatures within diverse bacterial lineages reflect adaptations related to growth and carbon utilization. From our bacterial culture collection isolated from experimental heated and control plots, we sequenced genomes representing dominant taxa sensitive to warming, including lineages of Actinobacteria, Alphaproteobacteria, and Betaproteobacteria. We investigated genomic attributes and functional gene content to identify signatures of adaptation. Comparative pangenomics revealed accessory gene clusters related to central metabolism, competition, and carbon substrate degradation, with few functional annotations explicitly associated with long-term warming. Trends in functional gene patterns suggest genomes from heated plots were relatively enriched in central carbohydrate and nitrogen metabolism pathways, while genomes from control plots were relatively enriched in amino acid and fatty acid metabolism pathways. We observed that genomes from heated plots had less codon bias, suggesting potential adaptive traits related to growth or growth efficiency. Codon usage bias varied for organisms with similar 16Srrnoperon copy number, suggesting that these organisms experience different selective pressures on growth efficiency. Our work suggests the emergence of lineage-specific trends as well as common ecological-evolutionary microbial responses to climate change.IMPORTANCEAnthropogenic climate change threatens soil ecosystem health in part by altering below-ground carbon cycling carried out by microbes. Microbial evolutionary responses are often overshadowed by community-level ecological responses, but adaptive responses represent potential changes in traits and functional potential that may alter ecosystem function. We predict that microbes are adapting to climate change stressors like soil warming. To test this, we analyzed the genomes of bacteria from a soil warming experiment where soil plots have been experimentally heated 5°C above ambient for over 30 years. While genomic attributes were unchanged by long-term warming, we observed trends in functional gene content related to carbon and nitrogen usage and genomic indicators of growth efficiency. These responses may represent new parameters in how soil ecosystems feedback to the climate system. 
    more » « less
  4. Marine microbes form the base of ocean food webs and drive ocean biogeochemical cycling. Yet little is known about the ability of microbial populations to adapt as they are advected through changing conditions. Here, we investigated the interplay between physical and biological timescales using a model of adaptation and an eddy-resolving ocean circulation climate model. Two criteria were identified that relate the timing and nature of adaptation to the ratio of physical to biological timescales. Genetic adaptation was impeded in highly variable regimes by nongenetic modifications but was promoted in more stable environments. An evolutionary trade-off emerged where greater short-term nongenetic transgenerational effects (low-γ strategy) enabled rapid responses to environmental fluctuations but delayed genetic adaptation, while fewer short-term transgenerational effects (high-γ strategy) allowed faster genetic adaptation but inhibited short-term responses. Our results demonstrate that the selective pressures for organisms within a single water mass vary based on differences in generation timescales resulting in different evolutionary strategies being favored. Organisms that experience more variable environments should favor a low-γ strategy. Furthermore, faster cell division rates should be a key factor in genetic adaptation in a changing ocean. Understanding and quantifying the relationship between evolutionary and physical timescales is critical for robust predictions of future microbial dynamics. 
    more » « less
  5. null (Ed.)
    Marine multicellular organisms host a diverse collection of bacteria, archaea, microbial eukaryotes, and viruses that form their microbiome. Such host-associated microbes can significantly influence the host’s physiological capacities; however, the identity and functional role(s) of key members of the microbiome (“core microbiome”) in most marine hosts coexisting in natural settings remain obscure. Also unclear is how dynamic interactions between hosts and the immense standing pool of microbial genetic variation will affect marine ecosystems’ capacity to adjust to environmental changes. Here, we argue that significantly advancing our understanding of how host-associated microbes shape marine hosts’ plastic and adaptive responses to environmental change requires (i) recognizing that individual host–microbe systems do not exist in an ecological or evolutionary vacuum and (ii) expanding the field toward long-term, multidisciplinary research on entire communities of hosts and microbes. Natural experiments, such as time-calibrated geological events associated with well-characterized environmental gradients, provide unique ecological and evolutionary contexts to address this challenge. We focus here particularly on mutualistic interactions between hosts and microbes, but note that many of the same lessons and approaches would apply to other types of interactions. 
    more » « less