Metabolism: Evolution retraces its steps to advance

  1. Daniel J Kliebenstein  Is a corresponding author
  1. University of California,Davis, United States

Selection can increase the fitness of a species in a stable environment by acting on random mutations. The same process can also create new traits if there is a change in the environment. Metabolism may evolve largely via the creation of new traits that either allow the organism to make use of new energy sources or provide new defense mechanisms in a complex environment (Blount et al. 2012; Prasad et al. 2012). However, we do not fully understand how new metabolic traits evolve or how they are integrated into existing metabolic networks.

Studying the creation of new traits is greatly complicated because evolution usually occurs over relatively long timescales. However, the Lenski long-term evolution experiment was designed to alleviate this problem and has been running at Michigan State University since 1988 (Fox and Lenski, 2015). Now, in eLife, Jeffrey Barrick and colleagues – including Erik Quandt as first author – make use of this resource to describe the molecular evolution of a new metabolic trait in E. coli (Quandt et al. 2015).

The long-term evolution experiment started with twelve identical populations of E. coli. These bacteria were forced to grow on culture medium that contained an excess of citrate, but very little glucose. Thus, for tens of thousands of generations of E. coli, the bacteria have been selected to evolve to use citrate as their main carbon source. This is something that E. coli would not normally do if they had access to oxygen. However, one of the populations did indeed evolve this exact ability (Blount et al. 2008; 2012). Sequencing the genome of this unique population throughout the long-term experiment identified the molecular changes that had generated this new trait. The new trait required two separate mutations within the gene that encodes an enzyme called citrate synthase (Quandt et al. 2015).

Barrick and colleagues – who are based at the University of Texas at Austin and Michigan State – now show that these two mutations have opposing effects (Quandt et al. 2015). The first mutation, called gltA1, abolished feedback inhibition in the enzyme and allowed the bacteria to use citrate, albeit weakly. This initial mutation was then followed by evolutionary shifts in genes that transcriptionally regulate primary metabolism (Leiby and Marx, 2014). Critically, this new transcriptional environment made the initial gltA1 mutation detrimental to fitness which, in turn, led to the rapid selection of variants of the citrate synthase gene that made the enzyme less active. Thus, while two opposing mutations within a single gene were required, they had to occur in a specific order and this order caused the mutations to be positive in both instances.

These new results show that the apparently unwavering march of evolution towards a new trait hides a meandering process underneath. In particular, they show that mutations that were at one time beneficial can consequently become a drag on fitness, and that mutations within existing genes can allow the creation of a new metabolic trait. This is in contrast to the standard view that the creation of new genes, often by gene duplication, is essential to the evolution of new metabolic traits (Chae et al. 2014; Wisecaver et al. 2014).

The use of the long-term evolution experiment has illuminated the complex mechanisms that allow adaptation to a consistent selective pressure in a single direction. However, it is possible that fluctuating and unpredictable stresses in the environment are more important drivers of evolution in nature (Kerwin et al. 2015), so there is a need for long-term experiments that include such stresses. The work of Quandt et al. represents, I hope, only the beginning of our ability to empirically study evolution in action.

References

Article and author information

Author details

  1. Daniel J Kliebenstein, Reviewing editor

    Department of Plant Sciences, University of California,Davis, Davis, United States
    For correspondence
    kliebenstein@ucdavis.edu
    Competing interests
    The author declares that no competing interests exist.

Publication history

  1. Version of Record published:

Copyright

© 2015, Kliebenstein

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,791
    views
  • 164
    downloads
  • 0
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Daniel J Kliebenstein
(2015)
Metabolism: Evolution retraces its steps to advance
eLife 4:e12386.
https://doi.org/10.7554/eLife.12386

Further reading

    1. Chromosomes and Gene Expression
    2. Evolutionary Biology
    Gülnihal Kavaklioglu, Alexandra Podhornik ... Christian Seiser
    Research Article

    Repression of retrotransposition is crucial for the successful fitness of a mammalian organism. The domesticated transposon protein L1TD1, derived from LINE-1 (L1) ORF1p, is an RNA-binding protein that is expressed only in some cancers and early embryogenesis. In human embryonic stem cells, it is found to be essential for maintaining pluripotency. In cancer, L1TD1 expression is highly correlative with malignancy progression and as such considered a potential prognostic factor for tumors. However, its molecular role in cancer remains largely unknown. Our findings reveal that DNA hypomethylation induces the expression of L1TD1 in HAP1 human tumor cells. L1TD1 depletion significantly modulates both the proteome and transcriptome and thereby reduces cell viability. Notably, L1TD1 associates with L1 transcripts and interacts with L1 ORF1p protein, thereby facilitating L1 retrotransposition. Our data suggest that L1TD1 collaborates with its ancestral L1 ORF1p as an RNA chaperone, ensuring the efficient retrotransposition of L1 retrotransposons, rather than directly impacting the abundance of L1TD1 targets. In this way, L1TD1 might have an important role not only during early development but also in tumorigenesis.

    1. Evolutionary Biology
    2. Genetics and Genomics
    Torsten Günther, Jacob Chisausky ... Cristina Valdiosera
    Research Article

    Cattle (Bos taurus) play an important role in the life of humans in the Iberian Peninsula not just as a food source but also in cultural events. When domestic cattle were first introduced to Iberia, wild aurochs (Bos primigenius) were still present, leaving ample opportunity for mating (whether intended by farmers or not). Using a temporal bioarchaeological dataset covering eight millennia, we trace gene flow between the two groups. Our results show frequent hybridisation during the Neolithic and Chalcolithic, likely reflecting a mix of hunting and herding or relatively unmanaged herds, with mostly male aurochs and female domestic cattle involved. This is supported by isotopic evidence consistent with ecological niche sharing, with only a few domestic cattle possibly being managed. The proportion of aurochs ancestry in domestic cattle remains relatively constant from about 4000 years ago, probably due to herd management and selection against first generation hybrids, coinciding with other cultural transitions. The constant level of wild ancestry (~20%) continues into modern Western European breeds including Iberian cattle selected for aggressiveness and fighting ability. This study illuminates the genomic impact of human actions and wild introgression in the establishment of cattle as one of the most important domestic species today.