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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Photorhabdus: a tale of contrasting interactions
More LessDifferent model systems have, over the years, contributed to our current understanding of the molecular mechanisms underpinning the various types of interaction between bacteria and their animal hosts. The genus Photorhabdus comprises Gram-negative insect pathogenic bacteria that are normally found as symbionts that colonize the gut of the infective juvenile stage of soil-dwelling nematodes from the family Heterorhabditis. The nematodes infect susceptible insects and release the bacteria into the insect haemolymph where the bacteria grow, resulting in the death of the insect. At this stage the nematodes feed on the bacterial biomass and, following several rounds of reproduction, the nematodes develop into infective juveniles that leave the insect cadaver in search of new hosts. Therefore Photorhabdus has three distinct and obligate roles to play during this life-cycle: (1) Photorhabdus must kill the insect host; (2) Photorhabdus must be capable of supporting nematode growth and development; and (3) Photorhabdus must be able to colonize the gut of the next generation of infective juveniles before they leave the insect cadaver. In this review I will discuss how genetic analysis has identified key genes involved in mediating, and regulating, the interaction between Photorhabdus and each of its invertebrate hosts. These studies have resulted in the characterization of several new families of toxins and a novel inter-kingdom signalling molecule and have also uncovered an important role for phase variation in the regulation of these different roles.
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Polyamines produced by Sinorhizobium meliloti Rm8530 contribute to symbiotically relevant phenotypes ex planta and to nodulation efficiency on alfalfa
More LessIn nitrogen-fixing rhizobia, emerging evidence shows significant roles for polyamines in growth and abiotic stress resistance. In this work we show that a polyamine-deficient ornithine decarboxylase null mutant (odc2) derived from Sinorhizobium meliloti Rm8530 had significant phenotypic differences from the wild-type, including greatly reduced production of exopolysaccharides (EPS; ostensibly both succinoglycan and galactoglucan), increased sensitivity to oxidative stress and decreased swimming motility. The introduction of the odc2 gene borne on a plasmid into the odc2 mutant restored wild-type phenotypes for EPS production, growth under oxidative stress and swimming. The production of calcofluor-binding EPS (succinoglycan) by the odc2 mutant was also completely or mostly restored in the presence of exogenous spermidine (Spd), norspermidine (NSpd) or spermine (Spm). The odc2 mutant formed about 25 % more biofilm than the wild-type, and its ability to form biofilm was significantly inhibited by exogenous Spd, NSpd or Spm. The odc2 mutant formed a less efficient symbiosis with alfalfa, resulting in plants with significantly less biomass and height, more nodules but less nodule biomass, and 25 % less nitrogen-fixing activity. Exogenously supplied Put was not able to revert these phenotypes and caused a similar increase in plant height and dry weight in uninoculated plants and in those inoculated with the wild-type or odc2 mutant. We discuss ways in which polyamines might affect the phenotypes of the odc2 mutant.
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Phylogenetic analyses of antibiotic-producing Streptomyces sp. isolates obtained from the stingless-bee Tetragonisca angustula (Apidae: Meliponini)
Many insects have been associated with actinobacteria in protective symbiosis where antimicrobial metabolites inhibit host pathogens. However, the microbiota of neotropical insects such as the stingless-bee Tetragonisca angustula is poorly explored. T. angustula is a meliponid bee widely distributed in Latin America, its honey is traditionally exploited because of its ethno-pharmacological properties and its antimicrobial activity has been demonstrated. Also, the well-structured nest of this species allows exploration of the microbiota of its different components. Even though Streptomyces spp. have been cultured from stingless-bees, little is known about their role in this insect–microbe relationship. In this study, we examined the association between culturable actinobacteria and T. angustula, and evaluated the isolates’ potential as antimicrobial producers. We isolated 51 actinobacteria from adult bees and different substrates of the hive of T. angustula (pollen and honey storage, garbage pellets and cerumen). We then performed a 16S rRNA phylogenetic analysis that clusters the bacteria to previously described lineages of host-associated Streptomyces . In addition, all the isolates were classified according to their antibacterial activity against human pathogens, measured by a growth inhibition test based on diffusion in agar. More than 50 % of our isolates exhibit antimicrobial activity, mainly to Gram-positive bacteria and fungi and only two against Gram-negative bacteria. Additionally, we obtained electron micrographs of adult bees with what appears to be patches of hyphae with Streptomyces -like cell morphology on their body surface. Our results suggest that T. angustula possibly uptakes and transfers actinobacteria from the environment, acting as vectors for these potentially beneficial organisms. This research provides new insights regarding the microbiota associated with T. angustula and justify future studies exploring the full diversity of the microbial community associated with the hive and the possible exchange of microbes with the crops they pollinate.
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Polyamines are required for normal growth in Sinorhizobium meliloti
More LessPolyamines (PAs) are ubiquitous polycations derived from basic l-amino acids whose physiological roles are still being defined. Their biosynthesis and functions in nitrogen-fixing rhizobia such as Sinorhizobium meliloti have not been extensively investigated. Thin layer chromatographic and mass spectrometric analyses showed that S. meliloti Rm8530 produces the PAs, putrescine (Put), spermidine (Spd) and homospermidine (HSpd), in their free forms and norspermidine (NSpd) in a form bound to macromolecules. The S. meliloti genome encodes two putative ornithine decarboxylases (ODC) for Put synthesis. Activity assays with the purified enzymes showed that ODC2 (SMc02983) decarboxylates both ornithine and lysine. ODC1 (SMa0680) decarboxylates only ornithine. An odc1 mutant was similar to the wild-type in ODC activity, PA production and growth. In comparison to the wild-type, an odc2 mutant had 45 % as much ODC activity and its growth rates were reduced by 42, 14 and 44 % under non-stress, salt stress or acid stress conditions, respectively. The odc2 mutant produced only trace levels of Put, Spd and HSpd. Wild-type phenotypes were restored when the mutant was grown in cultures supplemented with 1 mM Put or Spd or when the odc2 gene was introduced in trans. odc2 gene expression was increased under acid stress and reduced under salt stress and with exogenous Put or Spd. An odc1 odc2 double mutant had phenotypes similar to the odc2 mutant. These results indicate that ODC2 is the major enzyme for Put synthesis in S. meliloti and that PAs are required for normal growth in vitro.
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Physical contact and carbon transfer between a lichen-forming Trebouxia alga and a novel Alphaproteobacterium
More LessRecent progress in molecular techniques has begun to alter traditional recognition of lichens as symbiotic organisms comprised of a fungus and photosynthetic partners (green algae and/or cyanobacteria). Diverse organisms, especially various non-photosynthetic bacteria, are now indicated to be integral components of lichen symbiosis. Although lichen-associated bacteria are inferred to have functions that could support the symbiosis, little is known about their physical and nutritional interaction with fungi and algae. In the present study, we identified specific interaction between a lichen-forming alga and a novel bacterium. Trebouxia alga was isolated from a lichen, Usnea hakonensis, and kept as a strain for 8 years. Although no visible bacterial colonies were observed in this culture, high-throughput sequencing of DNA isolated from the culture revealed that the strain is composed of a Trebouxia alga and an Alphaproteobacterium species. In situ hybridization showed that bacterial cells were localized on the surface of the algal cells. Physiological assays revealed that the bacterium was able to use ribitol, glucose and mannitol, all of which are known to exist abundantly in lichens. It was resistant to three antibiotics. Bacteria closely related to this species were also identified in lichen specimens, indicating that U. hakonensis may commonly associate with this group of bacteria. These features of the novel bacterium suggest that it may be involved in carbon cycling of U. hakonensis as a member of lichen symbiosis and less likely to have become associated with the alga after isolation from a lichen.
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Phylogenetic clustering of Bradyrhizobium symbionts on legumes indigenous to North America
More LessTo analyse determinants of biogeographic structure in members of the genus Bradyrhizobium, isolates were obtained from 41 legume genera, originating from North American sites spanning 48.5 ° of latitude (Alaska to Panama). Sequencing of portions of six gene loci (3674 bp) in 203 isolates showed that there was only a weak trend towards higher nucleotide diversity in tropical regions. Phylogenetic relationships for nifD, in the symbiosis island region of the Bradyrhizobium chromosome, conflicted substantially with a tree inferred for five housekeeping gene loci. For both nifD and housekeeping gene trees, bacteria from each region were significantly more similar, on average, than would be expected if the source location was permuted at random on the tree. Within-region permutation tests also showed that bacteria clustered significantly on particular host plant clades at all levels in the phylogeny of legumes (from genus up to subfamily). Nevertheless, some bacterial groups were dispersed across multiple regions and were associated with diverse legume host lineages. These results indicate that migration, horizontal gene transfer and host interactions have all influenced the geographical divergence of Bradyrhizobium populations on a continental scale.
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Phylogenetic diversity of ‘Endomicrobia’ and their specific affiliation with termite gut flagellates
More Less‘Endomicrobia’, a distinct and diverse group of uncultivated bacteria in the candidate phylum Termite Group I (TG-1), have been found exclusively in the gut of lower termites and wood-feeding cockroaches. In a previous study, we had demonstrated that the ‘Endomicrobia’ clones retrieved from Reticulitermes santonensis represent intracellular symbionts of the two major gut flagellates of this termite. Here, we document that ‘Endomicrobia’ are present also in many other gut flagellates of lower termites. Phylogeny and host specificity of ‘Endomicrobia’ were investigated by cloning and sequencing of the small subunit rRNA genes of the flagellate and the symbionts, which originated from suspensions of individual flagellates isolated by micropipette. Each flagellate harboured a distinct phylogenetic lineage of ‘Endomicrobia’. The results of fluorescent in situ hybridization with ‘Endomicrobia’-specific oligonucleotide probes corroborated that ‘Endomicrobia’ are intracellular symbionts specifically affiliated with their flagellate hosts. Interestingly, the ‘Endomicrobia’ sequences obtained from flagellates belonging to the genus Trichonympha formed a monophyletic group, suggesting co-speciation between symbiont and host.
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Phage Induction of Lysogenic Rhizobium leguminosarum biovar trifolii in both the Free-living and the Symbiotic Form
More LessA lysogenic strain, Rhizobium leguminosarum biovar trifolii UK-1: φU, was isolated from a wild white clover nodule. It was symbiotically effective on white clover. A lysogenic phage (U-mole) was induced from this strain by treatment with either UV irradiation or mitomycin C. Phage U-mole had an icosahedral head (40 nm wide), a short tail (9 nm long) and tail fibres (15 nm long). Phage U-mole was induced with mitomycin C both from bacterial cells in infection threads and from bacteroids in nodules. Southern hybridization using EcoRI fragments of phage U-mole as probe indicated that phage U-mole DNA was integrated into the chromosome of strain UK-1: øU at a site involving the 60 kb EcoRI fragment of phage U-mole. Phage U-mole also lysogenized the wild-type strain R. leguminosarum biovar trifolii 4S. The resulting lysogenized strain, 4S:øU, had lost its 315 kb Sym plasmid and its nodulation ability.
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Plasmids and Symbiotic Effectiveness of Representative Phage Types from Two Indigenous Populations of Rhizobium meliloti
More LessSUMMARY: Phage types representative of the population of indigenous Rhizobium meliloti at each of two sites were evaluated for plasmid content by agarose gel electrophoresis and for symbiotic effectiveness with Medicago sativa cv. Saranac. Relative to four strains used commercially, 55 and 65 phage types representing these populations showed a high average level of symbiotic effectiveness; only a single type from one site was relatively ineffective in symbiosis. On the basis of plasmid number and molecular mass, 160 isolates comprising 45 and 48 types from both sites were placed in 22 different groups with 17 and 13 groups from the respective sites. The number of plasmids varied between one and five per isolate with molecular masses ranging from 5 MDa to considerably greater than 267 MDa. Only five isolates lacked a plasmid with mobility in agarose gels corresponding to that of a reference megaplasmid but instead showed a band of lesser mobility and therefore greater molecular mass. Phage types, which were divided into plasmid groups solely on the basis of differences between isolates from each site, may reflect adaptation of R. meliloti to their respective sites. Differences between isolates within certain phage types due to the presence or absence of a single plasmid may have resulted from genetic interchange between indigenous R. meliloti. There was no significant correlation between plasmid number or mass and symbiotic effectiveness or phage sensitivity of the phage types from either site.
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