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      Fitness costs and benefits vary for two facultative Burkholderia symbionts of the social amoeba, Dictyostelium discoideum

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          Abstract

          Hosts and their associated microbes can enter into different relationships, which can range from mutualism, where both partners benefit, to exploitation, where one partner benefits at the expense of the other. Many host–microbe relationships have been presumed to be mutualistic, but frequently only benefits to the host, and not the microbial symbiont, have been considered. Here, we address this issue by looking at the effect of host association on the fitness of two facultative members of the Dictyostelium discoideum microbiome ( Burkholderia agricolaris and Burkholderia hayleyella). Using two indicators of bacterial fitness, growth rate and abundance, we determined the effect of D. discoideum on Burkholderia fitness. In liquid culture, we found that D. discoideum amoebas lowered the growth rate of both Burkholderia species. In soil microcosms, we tracked the abundance of Burkholderia grown with and without D. discoideum over a month and found that B. hayleyella had larger populations when associating with D. discoideum while B. agricolaris was not significantly affected. Overall, we find that both B. agricolaris and B. hayleyella pay a cost to associate with D. discoideum, but B. hayleyella can also benefit under some conditions. Understanding how fitness varies in facultative symbionts will help us understand the persistence of host–symbiont relationships.

          OPEN RESEARCH BADGES

          This article has earned an Open Data Badge for making publicly available the digitally‐shareable data necessary to reproduce the reported results. The data is available at https://openscholarship.wustl.edu/data/15/

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          Most cited references53

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          Extreme genome reduction in symbiotic bacteria.

          Since 2006, numerous cases of bacterial symbionts with extraordinarily small genomes have been reported. These organisms represent independent lineages from diverse bacterial groups. They have diminutive gene sets that rival some mitochondria and chloroplasts in terms of gene numbers and lack genes that are considered to be essential in other bacteria. These symbionts have numerous features in common, such as extraordinarily fast protein evolution and a high abundance of chaperones. Together, these features point to highly degenerate genomes that retain only the most essential functions, often including a considerable fraction of genes that serve the hosts. These discoveries have implications for the concept of minimal genomes, the origins of cellular organelles, and studies of symbiosis and host-associated microbiota.
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            Transport and metabolism in legume-rhizobia symbioses.

            Symbiotic nitrogen fixation by rhizobia in legume root nodules injects approximately 40 million tonnes of nitrogen into agricultural systems each year. In exchange for reduced nitrogen from the bacteria, the plant provides rhizobia with reduced carbon and all the essential nutrients required for bacterial metabolism. Symbiotic nitrogen fixation requires exquisite integration of plant and bacterial metabolism. Central to this integration are transporters of both the plant and the rhizobia, which transfer elements and compounds across various plant membranes and the two bacterial membranes. Here we review current knowledge of legume and rhizobial transport and metabolism as they relate to symbiotic nitrogen fixation. Although all legume-rhizobia symbioses have many metabolic features in common, there are also interesting differences between them, which show that evolution has solved metabolic problems in different ways to achieve effective symbiosis in different systems.
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              Conditional outcomes in mutualistic interactions.

              Interspecific interactions are traditionally displayed in a grid in which each interaction is placed according to its outcome (positive, negative or neutral) for each partner. However, recent field studies consistently find the costs and benefits that determine net effects to vary greatly in both space and time, inevitably causing outcomes within most interactions to vary as well. Interactions show 'conditionality' when costs and benefits, and thus outcomes, are affected in predictable ways by current ecological conditions. The full range of natural outcomes of a given association may reveal far more about its ecological and evolutionary dynamics than does the average outcome at a given place and time. Copyright © 1994. Published by Elsevier Ltd.
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                Author and article information

                Contributors
                jrgarcia@nmhu.edu
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                15 August 2019
                September 2019
                : 9
                : 17 ( doiID: 10.1002/ece3.v9.17 )
                : 9878-9890
                Affiliations
                [ 1 ] Department of Biology Washington University in St. Louis St. Louis MO USA
                [ 2 ]Present address: Department of Biology New Mexico Highlands University Las Vegas NM USA
                Author notes
                [*] [* ] Correspondence

                Justine R. Garcia, Department of Biology, Washington University in St. Louis, St. Louis, MO 63130, USA.

                Email: jrgarcia@ 123456nmhu.edu

                Author information
                https://orcid.org/0000-0002-4183-1404
                Article
                ECE35529
                10.1002/ece3.5529
                6745654
                31534701
                07942763-a8ff-4c68-a5fd-87eaca0659d4
                © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 13 March 2019
                : 19 June 2019
                : 02 July 2019
                Page count
                Figures: 5, Tables: 1, Pages: 13, Words: 10488
                Funding
                Funded by: Division of Integrative Organismal Systems
                Award ID: IOS-1656756
                Funded by: John Templeton Foundation
                Award ID: 43667
                Funded by: Division of Environmental Biology
                Award ID: DEB-1753743
                Funded by: Washington University in St. Louis Institute of Clinical and Translational Science
                Award ID: NIH NCATS-UL1TR002345
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece35529
                September 2019
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.6.9 mode:remove_FC converted:16.09.2019

                Evolutionary Biology
                burkholderia,dictyostelium discoideum,host–microbe interaction,symbiont fitness,symbiosis

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