Intrasperm vertical symbiont transmission

Watanabe, Kenji; Yukuhiro, Fumiko; Matsuura, Yu; Fukatsu, Takema; Noda, Hiroaki

doi:10.1073/pnas.1402476111

Cited by 67 publications

(60 citation statements)

References 39 publications

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“…However, Wolbachia, also present in C. obscurior, could exert effects on host reproduction as well. In contrast to some other intracellular symbionts (Moran and Dunbar, 2006;Damiani et al, 2008;Watanabe et al, 2014), paternal transmission of Westeberhardia is unlikely as we did not detect Westeberhardia DNA in transferred sperm and/or seminal fluids stored in the spermatheca of uninfected queens mated to infected males.…”

Section: Transmission Of Westeberhardiacontrasting

confidence: 77%

A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior

et al. 2015

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The evolution of eukaryotic organisms is often strongly influenced by microbial symbionts that confer novel traits to their hosts. Here we describe the intracellular Enterobacteriaceae symbiont of the invasive ant Cardiocondyla obscurior, 'Candidatus Westeberhardia cardiocondylae'. Upon metamorphosis, Westeberhardia is found in gut-associated bacteriomes that deteriorate following eclosion. Only queens maintain Westeberhardia in the ovarian nurse cells from where the symbionts are transmitted to late-stage oocytes during nurse cell depletion. Functional analyses of the streamlined genome of Westeberhardia (533 kb, 23.41% GC content) indicate that neither vitamins nor essential amino acids are provided for the host. However, the genome encodes for an almost complete shikimate pathway leading to 4-hydroxyphenylpyruvate, which could be converted into tyrosine by the host. Taken together with increasing titers of Westeberhardia during pupal stage, this suggests a contribution of Westeberhardia to cuticle formation. Despite a widespread occurrence of Westeberhardia across host populations, one ant lineage was found to be naturally symbiont-free, pointing to the loss of an otherwise prevalent endosymbiont. This study yields insights into a novel intracellular mutualist that could play a role in the invasive success of C. obscurior.

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Section: Transmission Of Westeberhardiacontrasting

confidence: 77%

A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior

et al. 2015

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“…We consider that increasing the number of cells within the seeds could perhaps enable their use as autoinoculated seeds. The vertical transmission of symbiotic bacteria in plant and animal models is an important research field (55). It is necessary to know the determinants and the mechanism and genes responsible for this capability, in order to increase the rhizobial population in seeds and to reach a typical nitrogen-fixing symbiosis.…”

Section: Discussionmentioning

confidence: 99%

Nitrogen-Fixing Rhizobial Strains Isolated from Common Bean Seeds: Phylogeny, Physiology, and Genome Analysis

Mora

Dı́az

Vargas-Lagunas

et al. 2014

Appl Environ Microbiol

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Rhizobial bacteria are commonly found in soil but also establish symbiotic relationships with legumes, inhabiting the root nodules, where they fix nitrogen. Endophytic rhizobia have also been reported in the roots and stems of legumes and other plants. We isolated several rhizobial strains from the nodules of noninoculated bean plants and looked for their provenance in the interiors of the seeds. Nine isolates were obtained, covering most known bean symbiont species, which belong to the Rhizobium and Sinorhizobium groups. The strains showed several large plasmids, except for a Sinorhizobium americanum isolate. Two strains, one Rhizobium phaseoli and one S. americanum strain, were thoroughly characterized. Optimal symbiotic performance was observed for both of these strains. The S. americanum strain showed biotin prototrophy when subcultured, as well as high pyruvate dehydrogenase (PDH) activity, both of which are key factors in maintaining optimal growth. The R. phaseoli strain was a biotin auxotroph, did not grow when subcultured, accumulated a large amount of poly-␤-hydroxybutyrate, and exhibited low PDH activity. The physiology and genomes of these strains showed features that may have resulted from their lifestyle inside the seeds: stress sensitivity, a ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) complex, a homocitrate synthase (usually present only in free-living diazotrophs), a hydrogenase uptake cluster, and the presence of prophages. We propose that colonization by rhizobia and their presence in Phaseolus seeds may be part of a persistence mechanism that helps to retain and disperse rhizobial strains. Bacteria can populate diverse environments, from soil to water, even in the most extreme sites on the earth. These organisms can also be found on and inside other organisms, such as fungi, animals, and plants. The microbiome is a recently developed concept used to define the prokaryotic populations in close relationship with more-complex organisms (1, 2). Bacteria can flourish as endophytes inside plant roots, stems, leaves, and seeds (3) in crops (e.g., wheat, rice, maize, sorghum, and sugarcane), legumes (e.g., clover, common bean, and alfalfa), trees (e.g., Populus), grasses (e.g., switchgrass), and model plants (e.g., Arabidopsis) (4). Most common endophytic bacterial species have been described as members of the phyla Firmicutes and Proteobacteria (5).Legumes are economically valuable plants in agriculture and establish symbiotic relationships with rhizobial bacteria (6). These bacteria contribute to the formation of plant root nodules, colonizing them and fixing atmospheric nitrogen. This phenomenon has been studied intensively (7). Endophytic rhizobia, in tissues other than nodules, have also been isolated from clover and pea (e.g., Rhizobium phaseoli and Rhizobium leguminosarum bv. trifolii) (8). Several nonrhizobial bacterial species have been isolated from Phaseolus tissues (roots, stems, and seeds); these include Acinetobacter, Bacillus, Enterococcus, Nocardioides, Paracoccus, Phyll...

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“…In most cases, males are a dead end for symbionts (but see ref. 71), and symbionts are not expected to support male reproduction (72). Numerous cases of symbionts…”

Section: Increased Genetic Incompatabilitymentioning

confidence: 99%

Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

Bennett

Moran

2015

Proc. Natl. Acad. Sci. U.S.A.

415

515

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Many eukaryotes have obligate associations with microorganisms that are transmitted directly between generations. A model for heritable symbiosis is the association of aphids, a clade of sapfeeding insects, and Buchnera aphidicola, a gammaproteobacterium that colonized an aphid ancestor 150 million years ago and persists in almost all 5,000 aphid species. Symbiont acquisition enables evolutionary and ecological expansion; aphids are one of many insect groups that would not exist without heritable symbiosis. Receiving less attention are potential negative ramifications of symbiotic alliances. In the short run, symbionts impose metabolic costs. Over evolutionary time, hosts evolve dependence beyond the original benefits of the symbiosis. Symbiotic partners enter into an evolutionary spiral that leads to irreversible codependence and associated risks. Host adaptations to symbiosis (e.g., immune-system modification) may impose vulnerabilities. Symbiont genomes also continuously accumulate deleterious mutations, limiting their beneficial contributions and environmental tolerance. Finally, the fitness interests of obligate heritable symbionts are distinct from those of their hosts, leading to selfish tendencies. Thus, genes underlying the host-symbiont interface are predicted to follow a coevolutionary arms race, as observed for genes governing host-pathogen interactions. On the macroevolutionary scale, the rapid evolution of interacting symbiont and host genes is predicted to accelerate host speciation rates by generating genetic incompatibilities. However, degeneration of symbiont genomes may ultimately limit the ecological range of host species, potentially increasing extinction risk. Recent results for the aphidBuchnera symbiosis and related systems illustrate that, whereas heritable symbiosis can expand ecological range and spur diversification, it also presents potential perils.Buchnera | aphid | Muller's ratchet | selection levels | coevolution

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Intrasperm vertical symbiont transmission

Cited by 67 publications

References 39 publications

A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior

A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior

Nitrogen-Fixing Rhizobial Strains Isolated from Common Bean Seeds: Phylogeny, Physiology, and Genome Analysis

Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

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