Explaining microbial population genomics through phage predation

Rodrı́guez-Valera, Francisco; Martín-Cuadrado, Ana-Belén; Rodriguez-Brito, Beltrán; Pašić, Lejla; Thingstad, T. Frede; Rohwer, Forest; Mira, Álex

doi:10.1038/nrmicro2235

Cited by 566 publications

(396 citation statements)

References 66 publications

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“…These results could be attributable to different kinetics of the Tfd enzymes, e.g., enzymes with high versus low affinity for the substrate, or differential bacteriophage or protozoan predation of the abundant populations. The differential predation scenario has been well documented several times (33,(52)(53)(54), and preliminary findings reported by this study (discussed below) indicated that differential phage predation may be occurring in our mesocosms. However, whether or not this scenario fully applies to our mesocosm incubations remains to be experimentally tested.…”

Section: Discussionsupporting

confidence: 75%

“…Under such stressful conditions, lysogenic bacteriophages can transition to a lytic phase (55)(56)(57). Moreover, the patterns observed might also be attributed, at least partly, to a "kill the winner" scenario (52). Under this scenario, the most successful population, i.e., the one with efficient biodegradation genes under the growth conditions of our mesocosms, is preferentially targeted by bacteriophages.…”

Section: Discussionmentioning

confidence: 94%

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Quantifying the Importance of the Rare Biosphere for Microbial Community Response to Organic Pollutants in a Freshwater Ecosystem

Wang

Hatt

Tsementzi

et al. 2017

Appl Environ Microbiol

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A single liter of water contains hundreds, if not thousands, of bacterial and archaeal species, each of which typically makes up a very small fraction of the total microbial community (Ͻ0.1%), the so-called "rare biosphere." How often, and via what mechanisms, e.g., clonal amplification versus horizontal gene transfer, the rare taxa and genes contribute to microbial community response to environmental perturbations represent important unanswered questions toward better understanding the value and modeling of microbial diversity. We tested whether rare species frequently responded to changing environmental conditions by establishing 20-liter planktonic mesocosms with water from Lake Lanier (Georgia, USA) and perturbing them with organic compounds that are rarely detected in the lake, including 2,4-dichlorophenoxyacetic acid (2,4-D), 4-nitrophenol (4-NP), and caffeine. The populations of the degraders of these compounds were initially below the detection limit of quantitative PCR (qPCR) or metagenomic sequencing methods, but they increased substantially in abundance after perturbation. Sequencing of several degraders (isolates) and time-series metagenomic data sets revealed distinct cooccurring alleles of degradation genes, frequently carried on transmissible plasmids, especially for the 2,4-D mesocosms, and distinct species dominating the post-enrichment microbial communities from each replicated mesocosm. This diversity of species and genes also underlies distinct degradation profiles among replicated mesocosms. Collectively, these results supported the hypothesis that the rare biosphere can serve as a genetic reservoir, which can be frequently missed by metagenomics but enables community response to changing environmental conditions caused by organic pollutants, and they provided insights into the size of the pool of rare genes and species.IMPORTANCE A single liter of water or gram of soil contains hundreds of lowabundance bacterial and archaeal species, the so called rare biosphere. The value of this astonishing biodiversity for ecosystem functioning remains poorly understood, primarily due to the fact that microbial community analysis frequently focuses on abundant organisms. Using a combination of culture-dependent and culture-independent (metagenomics) techniques, we showed that rare taxa and genes commonly contribute to the microbial community response to organic pollutants. Our findings should have implications for future studies that aim to study the role of rare species in environmental processes, including environmental bioremediation efforts of oil spills or other contaminants.

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Section: Discussionsupporting

confidence: 75%

Section: Discussionmentioning

confidence: 94%

Quantifying the Importance of the Rare Biosphere for Microbial Community Response to Organic Pollutants in a Freshwater Ecosystem

Wang

Hatt

Tsementzi

et al. 2017

Appl Environ Microbiol

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“…According to the model proposed by Rodriguez-Valera et al (2009), the increase in abundance of a successful bacterial strain increases the chance of finding a phage specific to that strain (Lotka-Volterra dynamics). In this model, rare genotypes have a fitness advantage over abundant genotypes (i.e., kill-the-winner dynamics).…”

Section: Ecological Speciation With Phagesmentioning

confidence: 99%

Bacterial Diversification in the Light of the Interactions with Phages: The Genetic Symbionts and Their Role in Ecological Speciation

et al. 2018

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Phages have a major impact on microbial populations. In this work, we discuss how predation, transduction, lysogeny, and phage domestication lead to symbio-centric genomic interactions between bacteria and phages, ranging from antagonistic to mutualistic. Furthermore, these interactions influence bacterial diversification and ecotype formation. We then propose an additional consideration in the form of a symbio-centric ecological speciation framework for bacteria. Our framework builds upon classical morphological and molecular taxonomy by also considering bacteria and their phages as a unit of evolutionary selection. This framework acknowledges the considerable effect that phage interaction has on bacterial genomic content, regulation, and evolution, and will advance our understanding of bacterial evolution.

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“…Several authors have misinterpreted this kind of refutation as equivalent to a radical negation of any role of viruses in cell evolution [66,90]. However, it is important to stress that excluding viruses from the tree of life based on phylogenetic tests does not preclude the major role that viruses have played and still play in the evolution of cellular organisms acting as a strong and dynamic selective pressure on their hosts and fostering a permanent arms race [91]. Viruses are also important actors in cellular evolution by serving as vehicles for gene transfer and as accelerators of gene evolutionary rate ('mutators'), which may lead to punctual innovations that can be returned back to cells.…”

Section: Conclusion: the Vanishing 'Fourth Domain'mentioning

confidence: 99%

Evolution of viruses and cells: do we need a fourth domain of life to explain the origin of eukaryotes?

Moreira¹,

López‐García²

2015

Phil. Trans. R. Soc. B

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The recent discovery of diverse very large viruses, such as the mimivirus, has fostered a profusion of hypotheses positing that these viruses define a new domain of life together with the three cellular ones (Archaea, Bacteria and Eucarya). It has also been speculated that they have played a key role in the origin of eukaryotes as donors of important genes or even as the structures at the origin of the nucleus. Thanks to the increasing availability of genome sequences for these giant viruses, those hypotheses are amenable to testing via comparative genomic and phylogenetic analyses. This task is made very difficult by the high evolutionary rate of viruses, which induces phylogenetic artefacts, such as long branch attraction, when inadequate methods are applied. It can be demonstrated that phylogenetic trees supporting viruses as a fourth domain of life are artefactual. In most cases, the presence of homologues of cellular genes in viruses is best explained by recurrent horizontal gene transfer from cellular hosts to their infecting viruses and not the opposite. Today, there is no solid evidence for the existence of a viral domain of life or for a significant implication of viruses in the origin of the cellular domains.

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Explaining microbial population genomics through phage predation

Cited by 566 publications

References 66 publications

Quantifying the Importance of the Rare Biosphere for Microbial Community Response to Organic Pollutants in a Freshwater Ecosystem

Quantifying the Importance of the Rare Biosphere for Microbial Community Response to Organic Pollutants in a Freshwater Ecosystem

Bacterial Diversification in the Light of the Interactions with Phages: The Genetic Symbionts and Their Role in Ecological Speciation

Evolution of viruses and cells: do we need a fourth domain of life to explain the origin of eukaryotes?

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