Symbiosis
Symbiosis has played a key role in the evolution of life on Earth. Symbiotic mergers of once independent species drove the origin of eukaryotes. Moreover, symbiosis has enabled many species to gain novel functions and occupy new ecological niches, thus underpinning the functioning of diverse ecosystems. As endosymbionts, microbes provide their eukaryotic hosts with an array of ecological and physiological innovations, including new metabolic capabilities, such as autotrophy or nitrogen fixation, and protection against infections or environmental stressors. Microbial eukaryotes also commonly host their own endosymbionts, including bacteria and algae. Understanding the stability and resilience of symbioses is key to predicting the response of important ecosystems, such as coral reefs, to global change. Manipulating symbiotic associations also has far-reaching economic, environmental and medical implications, through the potential to improve crop productivity, reduce reliance on fertilisers, and control the insect vectors of infectious diseases.
This collection, guest edited by Professor Michael Brockhurst (University of Manchester) and Dr. Rebecca J Hall (University of Birmingham), will feature microbe-focused studies of symbiosis, ranging from the molecular mechanisms of host-symbiont interactions, their genetic and genomic diversity, to understanding the impacts of symbioses in natural and manmade ecosystems.
Collection Contents
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Symbiont-mediated immune priming in animals through an evolutionary lens
More LessProtective symbionts can defend hosts from parasites through several mechanisms, from direct interference to modulating host immunity, with subsequent effects on host and parasite fitness. While research on symbiont-mediated immune priming (SMIP) has focused on ecological impacts and agriculturally important organisms, the evolutionary implications of SMIP are less clear. Here, we review recent advances made in elucidating the ecological and molecular mechanisms by which SMIP occurs. We draw on current works to discuss the potential for this phenomenon to drive host, parasite, and symbiont evolution. We also suggest approaches that can be used to address questions regarding the impact of immune priming on host-microbe dynamics and population structures. Finally, due to the transient nature of some symbionts involved in SMIP, we discuss what it means to be a protective symbiont from ecological and evolutionary perspectives and how such interactions can affect long-term persistence of the symbiosis.
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Symbiont evolution during the free-living phase can improve host colonization
More LessFor micro-organisms cycling between free-living and host-associated stages, where reproduction occurs in both of these lifestyles, an interesting inquiry is whether evolution during the free-living stage can be positively pleiotropic to microbial fitness in a host environment. To address this topic, the squid host Euprymna tasmanica and the marine bioluminescent bacterium Vibrio fischeri were utilized. Microbial ecological diversification in static liquid microcosms was used to simulate symbiont evolution during the free-living stage. Thirteen genetically distinct V. fischeri strains from a broad diversity of ecological sources (e.g. squid light organs, fish light organs and seawater) were examined to see if the results were reproducible in many different genetic settings. Genetic backgrounds that are closely related can be predisposed to considerable differences in how they respond to similar selection pressures. For all strains examined, new mutations with striking and facilitating effects on host colonization arose quickly during microbial evolution in the free-living stage, regardless of the ecological context under consideration for a strain’s genetic background. Microbial evolution outside a host environment promoted host range expansion, improved host colonization for a micro-organism, and diminished the negative correlation between biofilm formation and motility.
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The Sinorhizobium meliloti sensor histidine kinase CbrA contributes to free-living cell cycle regulation
More LessSinorhizobium meliloti is alternately capable of colonizing the soil as a free-living bacterium or establishing a chronic intracellular infection with its legume host for the purpose of nitrogen fixation. We previously identified the S. meliloti two-component sensor histidine kinase CbrA as playing an important role in regulating exopolysaccharide production, flagellar motility and symbiosis. Phylogenetic analysis of CbrA has highlighted its evolutionary relatedness to the Caulobacter crescentus sensor histidine kinases PleC and DivJ, which are involved in CtrA-dependent cell cycle regulation through the shared response regulator DivK. We therefore became interested in testing whether CbrA plays a role in regulating S. meliloti cell cycle processes. We find the loss of cbrA results in filamentous cell growth accompanied by cells that contain an aberrant genome complement, indicating CbrA plays a role in regulating cell division and possibly DNA segregation. S. meliloti DivK localizes to the old cell pole during distinct phases of the cell cycle in a phosphorylation-dependent manner. Loss of cbrA results in a significantly decreased rate of DivK polar localization when compared with the wild-type, suggesting CbrA helps regulate cell cycle processes by modulating DivK phosphorylation status as a kinase. Consistent with a presumptive decrease in DivK phosphorylation and activity, we also find the steady-state level of CtrA increased in cbrA mutants. Our data therefore demonstrate that CbrA contributes to free-living cell cycle regulation, which in light of its requirement for symbiosis, points to the potential importance of cell cycle regulation for establishing an effective host interaction.
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The Sinorhizobium meliloti MsbA2 protein is essential for the legume symbiosis
Sinorhizobium meliloti is a beneficial legume symbiont, closely related to Brucella species, which are chronic mammalian pathogens. We discovered that the S. meliloti MsbA2 protein is essential to ensure the symbiotic interaction with the host plant, alfalfa. S. meliloti invades plant cells via plant-derived structures known as infection threads. However, in the absence of MsbA2, S. meliloti remains trapped within abnormally thickened infection threads and induces a heightened plant defence response, characterized by a substantial thickening of the nodule endodermis layer and the accumulation of polyphenolic compounds. The S. meliloti MsbA2 protein is homologous to the Escherichia coli lipopolysaccharide/phospholipid trafficking protein MsbA. However, MsbA2 was not essential for the membrane transport of either lipopolysaccharide or phospholipids in S. meliloti. We determined that the msbA2 gene is transcribed in free-living S. meliloti and that in the absence of MsbA2 the polysaccharide content of S. meliloti is altered. Consequently, we propose a model whereby the altered polysaccharide content of the S. meliloti msbA2 mutant could be responsible for its symbiotic defect by inducing an inappropriate host response.
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Sinorhizobium meliloti pSymB carries genes necessary for arabinose transport and catabolism
More LessArabinose is a known component of plant cell walls and is found in the rhizosphere. In this work, a previously undeleted region of the megaplasmid pSymB was identified as encoding genes necessary for arabinose catabolism, by Tn5-B20 random mutagenesis and subsequent complementation. Transcription of this region was measured by β-galactosidase assays of Tn5-B20 fusions, and shown to be strongly inducible by arabinose, and moderately so by galactose and seed exudate. Accumulation of [3H]arabinose in mutants and wild-type was measured, and the results suggested that this operon is necessary for arabinose transport. Although catabolite repression of the arabinose genes by succinate or glucose was not detected at the level of transcription, both glucose and galactose were found to inhibit accumulation of arabinose when present in excess. To determine if glucose was also taken up by the arabinose transport proteins, [14C]glucose uptake rates were measured in wild-type and arabinose mutant strains. No differences in glucose uptake rates were detected between wild-type and arabinose catabolism mutant strains, indicating that excess glucose did not compete with arabinose for transport by the same system. Arabinose mutants were tested for the ability to form nitrogen-fixing nodules on alfalfa, and to compete with the wild-type for nodule occupancy. Strains unable to utilize arabinose did not display any symbiotic defects, and were not found to be less competitive than wild-type for nodule occupancy in co-inoculation experiments. Moreover, the results suggest that other loci are required for arabinose catabolism, including a gene encoding arabinose dehydrogenase.
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Symbionts of the gut flagellate Staurojoenina sp. from Neotermes cubanus represent a novel, termite-associated lineage of Bacteroidales: description of ‘Candidatus Vestibaculum illigatum’
More LessThe symbioses between cellulose-degrading flagellates and bacteria are one of the most fascinating phenomena in the complex micro-ecosystem found in the hindgut of lower termites. However, little is known about the identity of the symbionts. One example is the epibiotic bacteria colonizing the surface of hypermastigote protists of the genus Staurojoenina. By using scanning electron microscopy, it was shown that the whole surface of Staurojoenina sp. from the termite Neotermes cubanus is densely covered with long rod-shaped bacteria of uniform size and morphology. PCR amplification of 16S rRNA genes from isolated protozoa and subsequent cloning yielded a uniform collection of clones with virtually identical sequences. Phylogenetic analysis placed them as a new lineage among the Bacteroidales, only distantly related to other uncultivated bacteria in the hindgut of other termites, including an epibiont of the flagellate Mixotricha paradoxa. The closest cultivated relative was Tannerella forsythensis (<85 % sequence identity). Fluorescence in situ hybridization with a newly designed clone-specific oligonucleotide probe confirmed that these sequences belong to the rod-shaped epibionts of Staurojoenina sp. Transmission electron microscopy confirmed the presence of a Gram-negative cell wall and revealed special attachment sites for the symbionts on the cell envelope of the flagellate host. Based on the isolated phylogenetic position and the specific association with the surface of Staurojoenina sp., we propose to classify this new taxon of Bacteroidales under the provisional name ‘Candidatus Vestibaculum illigatum’.
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Small genome of Candidatus Blochmannia, the bacterial endosymbiont of Camponotus, implies irreversible specialization to an intracellular lifestyle a
More LessaThe GenBank accession number for the sequence reported in this paper is AF495758.
Blochmannia (Candidatus Blochmannia gen. nov.) is the primary bacterial endosymbiont of the ant genus Camponotus. Like other obligate endosymbionts of insects, Blochmannia occurs exclusively within eukaryotic cells and has experienced long-term vertical transmission through host lineages. In this study, PFGE was used to estimate the genome size of Blochmannia as approximately 800 kb, which is significantly smaller than its free-living relatives in the enterobacteria. This small genome implies that Blochmannia has deleted most of the genetic machinery of related free-living bacteria. Due to restricted gene exchange in obligate endosymbionts, the substantial gene loss in Blochmannia and other insect mutualists may reflect irreversible specialization to a host cellular environment.
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Symbiotic Plasmid Rearrangement in a Hyper-recombinant Mutant of Rhizobium leguminosarum biovar phaseoli
More LessThe symbiotic plasmid of Rhizobium leguminosarum biovar phaseoli strain CFN23 has been previously shown to undergo a series of genetic rearrangements that modify the bacterial symbiotic phenotype. A hyper-recombinant derivative of strain CFN23 was isolated. This derivative (strain CFN2300) has a similar phenotype to that reported for Escherichia coli mutants defective in DNA metabolism. The frequency of CFN23 symbiotic plasmid deletion is increased in the CFN2300 background, suggesting that homologous genetic recombination is involved in the generation of this genetic rearrangement.
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Symbiotic Phenotypes of Auxotrophic Mutants of Rhizobium meliloti104A14
More LessAuxotrophic mutants of Rhizobium meliloti 104A14 were isolated using nitrous acid mutagenesis followed by penicillin enrichment. Mutants in ornithine transcarbamylase, argininosuccinate synthetase or serine-glycine biosynthesis formed nitrogen-fixing (Fix+) nodules on the roots of alfalfa (Medicago sativa). Mutants with defects in ornithine, pyrimidine, purine, asparagine, leucine, methionine or tyrosine biosynthesis, in one-carbon metabolism or in carbamoylphosphate synthetase formed nodules but these nodules were unable to fix nitrogen. Prototrophic revertants were always Fix+. Plasmids that would complement many of these auxotrophs were isolated by transduction with a P2 cosmid gene bank of R. meliloti 104A14. These plasmids were then introduced into mutants of the same and different classes and the growth and symbiotic phenotypes of the new strains were determined. In all cases, complementation of the nutritional defect restored symbiotic nitrogen fixation.
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Sugar Metabolism and the Symbiotic Properties of Carbohydrate Mutants of Rhizobium leguminosarum
More LessRhizobium leguminosarum metabolizes sugars via the Entner-Doudoroff and pentose phosphate pathways but does not have a functional Embden-Meyerhof pathway. Although some sugar catabolizing enzymes are constitutive, activities of the ‘Entner-Doudoroff’ enzymes vary with the carbon source. Bacteroids have complete pathways for sugar catabolism even though the specific activities of some enzymes, e.g., glucokinase, are lower than in free-living cells. Tn5-induced mutants lacking glucokinase, fructokinase and pyruvate dehydrogenase have been isolated. Although these mutants are unable to utilize sugars, they all nodulate peas and fix N2. The capacity to utilize particular C6 and C12 sugars is apparently not essential for bacteroid development or the establishment of effective N2 fixation.
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