Adaptation to environmental stress by evolution of non-genotypic heterogeneity within microbial populations

In order to survive in the natural environment, microorganisms must be able to cope with stresses arising from environmental change and perturbation. Sources of environmental stress include natural environmental pressures stemming from climate fluctuations and occasional exposure to harmful elements. In addition, pollution arising from human activities releases potentially-toxic contaminants. It is generally accepted that one key factor which helps species to survive such environmental stresses is the presence of 'genetic variation' within populations, arising from differences in DNA sequence among individual organisms of the same species. This variation means that individuals will have some slightly different characteristics, making it likely that some of the population will be better adapted to withstand particular stressful conditions and allow the species to survive. While such genetic variation is clearly very important, scientific advances over recent years have indicated that there is an additional factor important for the survival of environmental stresses. Experiments with single-cell microorganisms have shown that individual cells within a population have markedly different abilities to survive environmental stresses, despite having the same DNA composition (i.e. being genetically-uniform). This discovery has suggested that this new source of variation, known as 'non-genotypic heterogeneity', may be a major factor allowing microorganisms to survive and overcome environmental stress in nature. However, nearly all of the research into this topic has so far been performed only under model conditions with laboratory organisms. Our recent NERC-funded work has been the first to examine the importance of non-genotypic heterogeneity for microorganisms living in the natural environment, with extremely promising results.

Our studies to date have indicated that wild yeasts with high levels of non-genotypic heterogeneity have a competitive advantage over yeasts with lower heterogeneity in polluted habitats. Furthermore, these yeasts evolve the property of increased non-genotypic heterogeneity over time when subject to environmental stress. These important breakthroughs for microbial ecology underpin our new proposal. The objective now is to describe the wider importance of these exciting findings and, for the first time in wild cell populations selected by environmental stress, to uncover the mechanisms that underlie increased non-genotypic heterogeneity. We have three particular aims, as follows. (1) To determine how applicable our findings-to-date are more broadly. This will involve testing non-genotypic heterogeneity at environmental sites subject to quite diverse selection pressures as well as interrogation of a wide range of organisms, including bacteria. (2) To characterise the changes in DNA sequence that allow organisms to adapt to environmental stress by evolving increased non-genotypic heterogeneity. (3) To elucidate how these DNA sequence changes cause increased heterogeneity. We will adopt cutting-edge new techniques to achieve these objectives. The work could also have important applications, for example through the development of heterogeneity "markers" as novel biological reporters of pollutants in the natural environment. The results of the proposed project are anticipated to provide major new insights into non-genotypic heterogeneity as a survival strategy for species during environmental change. This will help greatly in our understanding of how microorganisms persist in the natural environment, and how they may react to harmful changes caused by humans through pollution.

Who will benefit from this research?

The principal economic and societal beneficiaries will be all those who gain from improved understanding of microbial diversity and survival in the natural environment; principally, the following: (1) Regulatory bodies concerned with environmental change and pollution. (2) Organizations providing environmental monitoring services. (3) Parties concerned with sustaining biodiversity in the environment. (4) The brewing, baking and other industries that exploit yeasts. (5) The general public. (6) Researchers and collaborators who are directly involved in the project.

How will they benefit from this research?

(1) With the increasing prominence of environmental issues for policy makers at government and inter-government levels, the improved understanding of impacts on organisms in the wild that this project will bring will help to guide the development of future policies on environmental change and pollution. As microorganisms are at the base of the food chain, new understanding of their responses to toxic pollutants also improves understanding of potential impacts on health of higher organisms including humans.

(2) It is anticipated that this project will reveal novel genetic markers of non-genotypic heterogeneity, with potential for application as innovative diagnostic probes of ecosystem health. Such assays have commercial value, and could be developed during the one to two years immediately following completion of the project.

(3) Biodiversity is a major scientific theme of the NERC and this project will fill a major gap in our understanding of biodiversity - the importance of non-genotypic heterogeneity for the survival of wild species during environmental change. Furthermore, this project will generate a library of wild microbial isolates all characterised for non-genotypic heterogeneity (diversity), from defined polluted and non-polluted locations across the UK. This will be a unique and valuable resource available to the broader community.

(4) The economic efficiency of industries like brewing and baking hinges strongly on optimal performance of the yeast that they use. Non-genotypic heterogeneity impacts this as only a subpopulation of cells may be performing optimally at any time. Although this proposal focuses on heterogeneity in the context of environmental stress, knowledge generated here could be exploited to help improve the efficiency of industrial operations with yeasts and so promote wealth generation.

(5) The proposed research is in an area that we have found appeals to the interests of the general public, from presentations we have given at University open days and outreach activities. Moreover, new awareness from this project will help to inform the public debate that contributes to environmental policy development.

(6) Staff working on this project will gain valuable new research skills as well as transferable skills like oral and written communication, collaboration, networking, and working as part of a team. The PDRA will receive specific exposure to science-to-policy initiatives and in communicating science to the public. These skills will improve their employment prospects in all sectors and their contribution to the economic competitiveness of the United Kingdom.