Antibiotic resistance in the wild: an eco-evolutionary perspective

The legacy of the use and misuse of antibiotics in recent decades has left us with a global public health crisis: antibiotic-resistant bacteria are on the rise, making it harder to treat infections. At the same time, evolution of antibiotic resistance is probably the best-documented case of contemporary evolution. To date, research on antibiotic resistance has largely ignored the complexity of interactions that bacteria engage in. However, in natural populations, bacteria interact with other species; for example, competition and grazing are import interactions influencing bacterial population dynamics. Furthermore, antibiotic leakage to natural environments can radically alter bacterial communities. Overall, we argue that eco-evolutionary feedback loops in microbial communities can be modified by residual antibiotics and evolution of antibiotic resistance. The aim of this review is to connect some of the well-established key concepts in evolutionary biology and recent advances in the study of eco-evolutionary dynamics to research on antibiotic resistance. We also identify some key knowledge gaps related to eco-evolutionary dynamics of antibiotic resistance, and review some of the recent technical advantages in molecular microbiology that offer new opportunities for tackling these questions. Finally, we argue that using the full potential of evolutionary theory and active communication across the different fields is needed for solving this global crisis more efficiently. This article is part of the themed issue ‘Human influences on evolution, and the ecological and societal consequences'.

[1]  R. MacLean,et al.  The SOS response increases bacterial fitness, but not evolvability, under a sublethal dose of antibiotic , 2015, Proceedings of the Royal Society B: Biological Sciences.

[2]  F. M. Stewart,et al.  The population genetics of antibiotic resistance. , 1997, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[3]  Riccardo Velasco,et al.  An evaluation of the PacBio RS platform for sequencing and de novo assembly of a chloroplast genome , 2013, BMC Genomics.

[4]  Johannes Cairns,et al.  Sublethal streptomycin concentrations and lytic bacteriophage together promote resistance evolution , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[5]  M. Perros.  A sustainable model for antibiotics , 2015, Science.

[6]  R. Lenski,et al.  Effect of Prey Heterogeneity on the Response of a Model Food Chain to Resource Enrichment , 1999, The American Naturalist.

[7]  Linus Sandegren,et al.  Selection of Resistant Bacteria at Very Low Antibiotic Concentrations , 2011, PLoS pathogens.

[8]  Giles Hooker,et al.  A newly discovered role of evolution in previously published consumer-resource dynamics. , 2014, Ecology letters.

[9]  Heather K. Allen,et al.  Call of the wild: antibiotic resistance genes in natural environments , 2010, Nature Reviews Microbiology.

[10]  Timothy A. Johnson,et al.  Diverse and abundant antibiotic resistance genes in Chinese swine farms , 2013, Proceedings of the National Academy of Sciences.

[11]  N. Pace.  A molecular view of microbial diversity and the biosphere. , 1997, Science.

[12]  A. Spiers,et al.  Plasmid carriage can limit bacteria–phage coevolution , 2015, Biology Letters.

[13]  Y. Carmeli,et al.  Epidemiological Interpretation of Studies Examining the Effect of Antibiotic Usage on Resistance , 2013, Clinical Microbiology Reviews.

[14]  C. Manaia,et al.  Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. , 2013, The Science of the total environment.

[15]  Tal Dagan,et al.  Trends and barriers to lateral gene transfer in prokaryotes. , 2011, Current opinion in microbiology.

[16]  E. Wellington,et al.  Incidence of Class 1 Integrons in a Quaternary Ammonium Compound-Polluted Environment , 2005, Antimicrobial Agents and Chemotherapy.

[17]  Robert C. Wolpert,et al.  A Review of the , 1985 .

[18]  Paul B Rainey,et al.  Antagonistic coevolution between a bacterium and a bacteriophage , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[19]  Robert D. Stedtfeld,et al.  High-throughput quantification of antibiotic resistance genes from an urban wastewater treatment plant. , 2016, FEMS microbiology ecology.

[20]  A. MacGowan,et al.  The role of pharmacokinetics/pharmacodynamics in setting clinical MIC breakpoints: the EUCAST approach. , 2012, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[21]  L. Becks,et al.  Consumer co-evolution as an important component of the eco-evolutionary feedback , 2014, Nature Communications.

[22]  Michael Travisano,et al.  Adaptive radiation in a heterogeneous environment , 1998, Nature.

[23]  Diarmaid Hughes,et al.  Antibiotic resistance and its cost: is it possible to reverse resistance? , 2010, Nature Reviews Microbiology.

[24]  D. Smith.  R factor infection of Escherichia coli lyophilized in 1946 , 1967, Journal of bacteriology.

[25]  M. Ward,et al.  Sources of Antimicrobial Resistance , 2013, Science.

[26]  Erik Kristiansson,et al.  Shotgun metagenomics reveals a wide array of antibiotic resistance genes and mobile elements in a polluted lake in India , 2014, Front. Microbiol..

[27]  P. Blainey.  The future is now: single-cell genomics of bacteria and archaea. , 2013, FEMS microbiology reviews.

[28]  Silvia Berkner,et al.  Antibiotic resistance and the environment—there and back again , 2014, EMBO reports.

[29]  Adrian W. Briggs,et al.  Massively parallel sequencing of single cells by epicPCR links functional genes with phylogenetic markers , 2015, The ISME Journal.

[30]  M. Duffy,et al.  Human drivers of ecological and evolutionary dynamics in emerging and disappearing infectious disease systems , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[31]  D. Andersson,et al.  Evolution of antibiotic resistance at non-lethal drug concentrations. , 2012, Drug resistance updates : reviews and commentaries in antimicrobial and anticancer chemotherapy.

[32]  A. Phillimore,et al.  Species Interactions Alter Evolutionary Responses to a Novel Environment , 2012, PLoS biology.

[33]  A. Magurran.  The Ecological Theater , 2009, Science.

[34]  Alexander S. Mikheyev,et al.  A first look at the Oxford Nanopore MinION sequencer , 2014, Molecular ecology resources.

[35]  Diarmaid Hughes,et al.  Microbiological effects of sublethal levels of antibiotics , 2014, Nature Reviews Microbiology.

[36]  D. Reznick.  A Critical Look at Reciprocity in Ecology and Evolution: Introduction to the Symposium* , 2013, The American Naturalist.

[37]  John Bunge,et al.  Predicting microbial species richness. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[38]  M E Woolhouse,et al.  Risk factors for human disease emergence. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[39]  Stephan Harbarth,et al.  Antibiotic Selection Pressure and Resistance in Streptococcus pneumoniae and Streptococcus pyogenes , 2004, Emerging infectious diseases.

[40]  T. Schoener.  The Newest Synthesis: Understanding the Interplay of Evolutionary and Ecological Dynamics , 2011, Science.

[41]  Remy Chait,et al.  Evolutionary paths to antibiotic resistance under dynamically sustained drug selection , 2011, Nature Genetics.

[42]  N. Datta,et al.  Conjugative plasmids in bacteria of the ‘pre-antibiotic’ era , 1983, Nature.

[43]  M. Gillings,et al.  Are humans increasing bacterial evolvability? , 2012, Trends in ecology & evolution.

[44]  Molly K. Gibson,et al.  Bacterial phylogeny structures soil resistomes across habitats , 2014, Nature.

[45]  H. Ochman,et al.  Long-Term Shifts in Patterns of Antibiotic Resistance in Enteric Bacteria , 2000, Applied and Environmental Microbiology.

[46]  Klaus Kümmerer,et al.  Antibiotics in the aquatic environment--a review--part I. , 2009, Chemosphere.

[47]  Timothy E. Farkas,et al.  Evolution of Camouflage Drives Rapid Ecological Change in an Insect Community , 2013, Current Biology.

[48]  A O Summers,et al.  Mercury released from dental "silver" fillings provokes an increase in mercury- and antibiotic-resistant bacteria in oral and intestinal floras of primates , 1993, Antimicrobial Agents and Chemotherapy.

[49]  C. Kimmel.  Introduction to the symposium. , 1997, Reproductive toxicology.

[50]  K. Kümmerer.  Antibiotics in the aquatic environment--a review--part II. , 2009, Chemosphere.

[51]  D. Livermore,et al.  Fourteen years in resistance. , 2012, International journal of antimicrobial agents.

[52]  H. Giamarellou,et al.  Multidrug-resistant and extensively drug-resistant Gram-negative pathogens: current and emerging therapeutic approaches , 2014, Expert opinion on pharmacotherapy.

[53]  Troy Day,et al.  Does High-Dose Antimicrobial Chemotherapy Prevent the Evolution of Resistance? , 2016, PLoS Comput. Biol..

[54]  Charles W. Knapp,et al.  Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. , 2010, Environmental science & technology.

[55]  Ramunas Stepanauskas,et al.  Co-selection of antibiotic and metal resistance. , 2006, Trends in microbiology.

[56]  G. E. Hutchinson,et al.  The ecological theater and the evolutionary play , 1965 .

[57]  J. Farrar,et al.  Antimicrobial resistance in humans, livestock and the wider environment , 2015, Philosophical Transactions of the Royal Society B: Biological Sciences.

[58]  Janis Antonovics,et al.  Evolution by Any Other Name: Antibiotic Resistance and Avoidance of the E-Word , 2007, PLoS Biology.

[59]  Alex R. Hall,et al.  The population genetics of antibiotic resistance: integrating molecular mechanisms and treatment contexts , 2010, Nature Reviews Genetics.

[60]  P. Hawkey,et al.  The changing epidemiology of resistance. , 2009, The Journal of antimicrobial chemotherapy.

[61]  D. G. Joakim Larsson,et al.  Pollution from drug manufacturing: review and perspectives , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[62]  S. Ellner,et al.  Rapid evolution and the convergence of ecological and evolutionary time , 2005 .

[63]  A. Hendry,et al.  Eco-evolutionary dynamics , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[64]  A. Hendry,et al.  Cryptic eco‐evolutionary dynamics , 2015, Annals of the New York Academy of Sciences.

[65]  M. Brockhurst,et al.  Conjugation is necessary for a bacterial plasmid to survive under protozoan predation , 2016, Biology Letters.

[66]  Marco Fondi,et al.  Large-scale analysis of plasmid relationships through gene-sharing networks. , 2012, Molecular biology and evolution.