Comment pubs.acs.org/est
Guest Comment: Environmental Genomics Focus Issue
G
enome science is already witnessing the second revolution in its still short lifetime: the introduction of next-generation sequencing technologies. These new technologies, of which four major platforms are presently in use, can generate so much nucleotide sequence data so rapidly and at such low costs that application to species outside the standard genetic models becomes feasible. In the early days of genomics, attention was mostly focused on the full genome sequences of a few model organisms (“yeast, fly, worm, and weed”). Now, only 10 years after closing the genome sequence of the nematode C. elegans (November 2002), genome sequencing of “genetically naive” organisms, even with large genomes, is no longer limiting biological analysis. For example, a genome sequence for the giant panda was published in 2010; this was the first complex genome to be assembled de novo exclusively from next-generation sequencing data. With this tremendous increase in throughput, not only did the sequencing of ecologically relevant organisms with littleknown genomes become possible, but also the genomic exploration of entire communities from field samples or enrichment cultures. In this “metagenomics” approach, first exemplified by Craig Venter’s 2004 work on the Sargasso Sea, environmental DNA is sequenced without regard to its source species. In several cases the genomes of species that had never been cultured nor morphologically described have been assembled. For example, in 2006 the genome of the anammox bacterium Kuenenia stuttgartiensis was assembled from a metagenomic sequencing effort applied to a bioreactor community. Genome technology invaded environmental sciences around the beginning of the century and was marked by a 2003 Gordon Research Conference on “Evolutionary and Ecological Functional Genomics”. Since then, its influence has grown steadily in environmental science journals, including Environmental Science and Technology. “Ecological genomics”, “ecogenomics”, or “environmental genomics”, as it is variously called, has developed into a true subdiscipline of environmental science, with dedicated sessions in conferences and the first textbook published in 2006. For environmental science the crucial question is how genomic insights can improve our understanding of the risks of potentially toxic chemicals. The papers collected for this Focus Issue illustrate the great variety of approaches to this question. The studies concern questions related to wastewater treatment, soil and terrestrial toxicity, aquatic toxicity, and biodegradation. One recurrent theme in environmental genomics is the characterization of the mode of action of chemicals using genome-wide gene expression. Gene expression profiles represent an immensely rich source of information on the biochemical processes influenced (upregulated or downregulated) by exposure to chemicals. These profiles, as argued in this issue by Van Straalen & Feder are highly specific to the chemical, even when closely related chemicals are compared. This is nicely illustrated by the paper by Dom and others on Daphnia exposed to narcotic and polar narcotic compounds. In © 2011 American Chemical Society
addition, some genes are closely linked to the body residue, as Gong and others show for earthworms exposed to explosives. Furthermore, Teraoka and others, in a study on chicken and common cormorant exposed to dioxin, show that the transcriptomic response to toxicants may involve unexpected, novel genes, suggesting new toxicant-specific markers of exposure. In addition, Zhao and others show that toxicity mechanisms may involve not only protein-encoding genes, but also microRNAs. Effects of toxicants on levels of microRNAs will not be revealed by classical transcriptomics approaches, which examine only mRNA. Up to now environmental genomics has focused on exposure to one chemical at a time. Garcia-Reyero et al. exposed Daphnia to mixtures of munition constituents and contaminated groundwater. In this issue they show that in the transcriptome, addditive and nonadditive effects may interact in such a complicated way that estimation of the composition of mixtures from gene expression profiles becomes extremely difficult. In addition, the transcriptomic responses need not be monotonic with dose, as Villeneuve and others illustrate for two species of fish. This poses a problem for risk assessment, because monotony between dose and biological response is a crucial assumption when setting thresholds or standards. Maximum acceptable concentrations of chemicals in the environment are commonly derived from indices such as NOECs or EC50s; if such indices are not apparent at the transcriptome level, the application of transcriptomics to quantitative risk assessment becomes problematic. It is still possible, however, to discriminate environmental samples based on biological responses. The contributions by De Boer and others on copper-contaminated soils and by VidalDorsch and others, on contaminated estuarine wetlands illustrate this. Zhang and others were able to show that Yangtze River water, when used as a source of drinking water for mice, resulted in a gene expression profile characteristic of upregulated xenobiotic metabolism, indicating the presence of chemicals with biological effects. All these studies provide strong support for transcriptomics as a sensitive, extremely specific, and rapid source of information on the chemicals to which a test organism is exposed. In a different way, the same principle applies to microbial communities. Günther and others show that the rapidly changing community of a wastewater treatment plant can be monitored with a combination of flow cytometry and molecular fingerprinting. A possible application of this work is that the control unit of the plant can be fed with useful biological information on the wastewater treatment process. Genomics technology can also be used to track the sources of enteric bacteria in surface water that impact the quality of waterways, as Unno and others in this Focus issue illustrate. The diversity of approaches in environmental genomics is further illustrated by a contribution from DeBruyn and others, on the aromatic ring Special Issue: Ecogenomics: Environmental Published: December 12, 2011 1
dx.doi.org/10.1021/es204242a | Environ. Sci. Technol. 2012, 46, 1−2
Environmental Science & Technology
Comment
hydroxylating dioxygenase genes that allow a bacterium to degrade polycyclic aromatic hydrocarbons. The authors suggest that these genes have been subject to lateral gene transfer, conferring PAH degradation to a phylogenetically disparate set of microbial lineages. Environmental genomics is growing with ongoing acceleration. Technological revolutions are having and will continue to have a major impact. On this high-speed track, the imperative for scientists and risk assessors to sit together and interact becomes even greater.
research paradigm, and he cofounded the Gordon Research Conference on this topic in 2003.
Nico M. van Straalen* Martin E. Feder Gary S. Sayler
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Gary S. Sayler, ES&T Associate Editor, is a Beaman Distinguished Professor of Microbiology at the University of Tennessee, Knoxville. He is the founding director of the University of Tennessee Center for Environmental Biotechnology and director of the UTORNL Joint Institute for Biological Sciences. With over 35 years of experience in multidisciplinary laboratory and field environmental research and biodegradation of organic pollutants, he pioneered the development of environmental molecular diagnostics, including the extraction and analysis of nucleic acids from soils, environmental gene probe analysis, bioluminescent bioreporter technology, and the first field release of a genetically engineered microorganism for remediation purposes. He is past Chairman of EPA/ORD Board of Scientific Counselors and currently serves on the SERDP Advisory Board and DOE’s BERAC.
AUTHOR INFORMATION
Corresponding Author *E-mail:
[email protected]. Biographies
Nico M. van Straalen is a professor of Animal Ecology at VU University, Amsterdam, where he teaches evolutionary biology, animal physiology, ecology, and environmental toxicology. His research interests concern the evolution of toxicant tolerance in soilliving invertebrates, and the molecular mechanisms involved. His laboratory developed genomics resources for the collembolan Folsomia candida, a model species for soil toxicity testing. With Dick Roelofs he wrote a textbook “An Introduction to Ecological Genomics” (OUP, 2nd Ed., 2012). In the past Nico van Straalen has contributed to risk assessment methodology by introducing the species-sensitivity distribution approach. He served in the founding board of SETACEurope.
Martin E. Feder is the Elise and Jack Lipsey Professor and Faculty Dean in the Division of Biological Sciences at The University of Chicago. He earned a Ph.D. degree from the University of California, Berkeley. In a first phase of research, he studied the regulation and evolutionary implications of cutaneous exchange in vertebrates, and more generally evolutionary physiology. Later research took up the environmental control of gene and protein expression, and used the heat-shock response in Drosophila as a model. This work led to advocacy of ecological and evolutionary functional genomics as a 2
dx.doi.org/10.1021/es204242a | Environ. Sci. Technol. 2012, 46, 1−2
