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      Exploiting rRNA Operon Copy Number to Investigate Bacterial Reproductive Strategies

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      1 , 2 , 1 , 1 , 3 , 4 , *
      Nature microbiology

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          Summary

          The potential for rapid reproduction is a hallmark of microbial life, but microbes in nature must also survive and compete when growth is constrained by resource availability. Successful reproduction requires different strategies when resources are scarce compared to when they are abundant 1, 2 , but a systematic framework for predicting these reproductive strategies in bacteria has not been available. Here we show that the number of ribosomal RNA operons ( rrn) in bacterial genomes predicts two important components of reproduction – growth rate and growth efficiency – which are favored under contrasting regimes of resource availability 3, 4 . We find that the maximum reproductive rate of bacteria doubles with a doubling of rrn copy number, while the efficiency of carbon use is inversely related to maximal growth rate and rrn copy number. We also identify a feasible explanation for these patterns: the rate and yield of protein synthesis mirror the overall pattern in maximum growth rate and growth efficiency. Furthermore, comparative analysis of genomes from 1,167 bacterial species reveals that rrn copy number predicts traits associated with resource availability, including chemotaxis and genome streamlining. Genome-wide patterns of orthologous gene content covary with rrn copy number, suggesting convergent evolution in response to resource availability. Our findings indicate that basic cellular processes adapt in contrasting ways to long-term differences in resource availability. They also establish a basis for predicting changes in bacterial community composition in response to resource perturbations using rrn copy number measurements 5 or inferences 6, 7 .

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          The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss

          ABSTRACT Reductive genomic evolution, driven by genetic drift, is common in endosymbiotic bacteria. Genome reduction is less common in free-living organisms, but it has occurred in the numerically dominant open-ocean bacterioplankton Prochlorococcus and “Candidatus Pelagibacter,” and in these cases the reduction appears to be driven by natural selection rather than drift. Gene loss in free-living organisms may leave them dependent on cooccurring microbes for lost metabolic functions. We present the Black Queen Hypothesis (BQH), a novel theory of reductive evolution that explains how selection leads to such dependencies; its name refers to the queen of spades in the game Hearts, where the usual strategy is to avoid taking this card. Gene loss can provide a selective advantage by conserving an organism’s limiting resources, provided the gene’s function is dispensable. Many vital genetic functions are leaky, thereby unavoidably producing public goods that are available to the entire community. Such leaky functions are thus dispensable for individuals, provided they are not lost entirely from the community. The BQH predicts that the loss of a costly, leaky function is selectively favored at the individual level and will proceed until the production of public goods is just sufficient to support the equilibrium community; at that point, the benefit of any further loss would be offset by the cost. Evolution in accordance with the BQH thus generates “beneficiaries” of reduced genomic content that are dependent on leaky “helpers,” and it may explain the observed nonuniversality of prototrophy, stress resistance, and other cellular functions in the microbial world.
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            rRNA operon copy number reflects ecological strategies of bacteria.

            Although natural selection appears to favor the elimination of gene redundancy in prokaryotes, multiple copies of each rRNA-encoding gene are common on bacterial chromosomes. Despite this conspicuous deviation from single-copy genes, no phenotype has been consistently associated with rRNA gene copy number. We found that the number of rRNA genes correlates with the rate at which phylogenetically diverse bacteria respond to resource availability. Soil bacteria that formed colonies rapidly upon exposure to a nutritionally complex medium contained an average of 5.5 copies of the small subunit rRNA gene, whereas bacteria that responded slowly contained an average of 1.4 copies. In soil microcosms pulsed with the herbicide 2,4-dichlorophenoxyacetic acid (2,4-D), indigenous populations of 2,4-D-degrading bacteria with multiple rRNA genes ( = 5.4) became dominant, whereas populations with fewer rRNA genes ( = 2.7) were favored in unamended controls. These findings demonstrate phenotypic effects associated with rRNA gene copy number that are indicative of ecological strategies influencing the structure of natural microbial communities.
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              R: language and environment for statistical computing

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                Author and article information

                Journal
                101674869
                44774
                Nat Microbiol
                Nat Microbiol
                Nature microbiology
                2058-5276
                19 August 2016
                12 September 2016
                2016
                12 March 2017
                : 1
                : 16160
                Affiliations
                [1 ] Department of Internal Medicine, University of Michigan, Ann Arbor, MI, 48109, USA
                [2 ] Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, 48824, USA
                [3 ] Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, 48109, USA
                [4 ] Department of Microbiology and Immunology, University of Michigan, Ann Arbor, MI, 48109, USA
                Author notes
                [+]

                Current address: Center for Adaptation to a Changing Environment, ETH Zürich, 8092 Zürich, Switzerland

                [* ] To whom correspondence should be addressed. Tel: 1-(734)-763-8206; Fax: 1-(734)-615-5534; schmidti@ 123456umich.edu
                Article
                NIHMS807913
                10.1038/nmicrobiol.2016.160
                5061577
                27617693
                12388821-699e-4bf4-a14d-7111acf15d7c

                Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms

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