Dual Symbiosis Research Articles

Flexibility in Aphid Endosymbiosis: Dual Symbioses Have Evolved Anew at Least Six Times

Flexibility in Aphid Endosymbiosis: Dual Symbioses Have Evolved Anew at Least Six Times

Novel symbionts and potential human pathogens excavated from argasid tick microbiomes that are shaped by dual or single symbiosis

Research on vector-associated microbiomes has been expanding due to increasing emergence of vector-borne pathogens and awareness of the importance of symbionts in the vector physiology. However, little is known about microbiomes of argasid (or soft-bodied) ticks due to limited access to specimens. We collected four argasid species (Argas japonicus, Carios vespertilionis, Ornithodoros capensis, and Ornithodoros sawaii) from the nests or burrows of their vertebrate hosts. One laboratory-reared argasid species (Ornithodoros moubata) was also included. Attempts were then made to isolate and characterize potential symbionts/pathogens using arthropod cell lines. Microbial community structure was distinct for each tick species. Coxiella was detected as the predominant symbiont in four tick species where dual symbiosis between Coxiella and Rickettsia or Coxiella and Francisella was observed in C. vespertilionis and O. moubata, respectively. Of note, A. japonicus lacked Coxiella and instead had Occidentia massiliensis and Thiotrichales as alternative symbionts. Our study found strong correlation between tick species and life stage. We successfully isolated Oc. massiliensis and characterized potential pathogens of genera Ehrlichia and Borrelia. The results suggest that there is no consistent trend of microbiomes in relation to tick life stage that fit all tick species and that the final interpretation should be related to the balance between environmental bacterial exposure and endosymbiont ecology. Nevertheless, our findings provide insights on the ecology of tick microbiomes and basis for future investigations on the capacity of argasid ticks to carry novel pathogens with public health importance.

Evolutionarily recent dual obligatory symbiosis among adelgids indicates a transition between fungus- and insect-associated lifestyles

Adelgids (Insecta: Hemiptera: Adelgidae) form a small group of insects but harbor a surprisingly diverse set of bacteriocyte-associated endosymbionts, which suggest multiple replacement and acquisition of symbionts over evolutionary time. Specific pairs of symbionts have been associated with adelgid lineages specialized on different secondary host conifers. Using a metagenomic approach, we investigated the symbiosis of the Adelges laricis/Adelgestardus species complex containing betaproteobacterial (“Candidatus Vallotia tarda”) and gammaproteobacterial (“Candidatus Profftia tarda”) symbionts. Genomic characteristics and metabolic pathway reconstructions revealed that Vallotia and Profftia are evolutionary young endosymbionts, which complement each other’s role in essential amino acid production. Phylogenomic analyses and a high level of genomic synteny indicate an origin of the betaproteobacterial symbiont from endosymbionts of Rhizopus fungi. This evolutionary transition was accompanied with substantial loss of functions related to transcription regulation, secondary metabolite production, bacterial defense mechanisms, host infection, and manipulation. The transition from fungus to insect endosymbionts extends our current framework about evolutionary trajectories of host-associated microbes.

Hologenome analysis reveals dual symbiosis in the deep-sea hydrothermal vent snail Gigantopelta aegis

Animals endemic to deep-sea hydrothermal vents often form obligatory symbioses with bacteria, maintained by intricate host–symbiont interactions. Most genomic studies on holobionts have not investigated both sides to similar depths. Here, we report dual symbiosis in the peltospirid snail Gigantopelta aegis with two gammaproteobacterial endosymbionts: a sulfur oxidiser and a methane oxidiser. We assemble high-quality genomes for all three parties, including a chromosome-level host genome. Hologenomic analyses reveal mutualism with nutritional complementarity and metabolic co-dependency, highly versatile in transporting and using chemical energy. Gigantopelta aegis likely remodels its immune system to facilitate dual symbiosis. Comparisons with Chrysomallon squamiferum, a confamilial snail with a single sulfur-oxidising gammaproteobacterial endosymbiont, show that their sulfur-oxidising endosymbionts are phylogenetically distant. This is consistent with previous findings that they evolved endosymbiosis convergently. Notably, the two sulfur-oxidisers share the same capabilities in biosynthesising nutrients lacking in the host genomes, potentially a key criterion in symbiont selection.

Benefits of dual inoculation with arbuscular mycorrhizal fungi and rhizobia on Phaseolus vulgaris planted in a low-fertility tropical soil

The growth response of Phaseolus vulgaris to dual inoculation with arbuscular mycorrhizal (AM) fungi and rhizobia was studied in a low-fertility tropical soil in Madagascar. Two isolates of AM fungi identified as Acaulospora sp. and Glomus sp., respectively, along with a cocktail of ten Rhizobium spp. strains were used to conduct a greenhouse experiment in a fully randomized block design with two factors. The Phaseolus vulgaris seedlings received one of the following inoculation treatments: no inoculation, separate inoculation with each of the three microbial symbionts (the two AM fungal isolates and the rhizobia), and co-inoculation with each of the two AM fungal isolates and the mix of rhizobium strains. The results showed an additive effect of co-infection by AM fungi and rhizobia on plant growth and on the total N content of the plants, along with a synergistic effect on the total P content, the number of nodules and the mycorrhizal rate of the plants. Dual symbiosis with native strains contributes to the success of legumes, especially in harsh environments and low-fertility tropical soils.

Interaction between Piriformospora indica and Azotobacter chroococcum diminish the effect of salt stress in Artemisia annua L. by enhancing enzymatic and non-enzymatic antioxidants

Artemisia annua is a medicinal plant known for artemisinin, a potential anti-malarial drug. In this study, we investigated how the mutualistic and synergistic interaction between Piriformospora indica (Pi) and Azotobacter chroococcum (Az) ameliorates the damaging effects of salinity on A. annua L. Our findings revealed that dual treated plants had better plant height, dry weights of shoot and root under salt stress than the un-inoculated ones. During salt stress, microbial treated plants reduced the oxidative damage in plants by decreasing the concentrations of MDA [Pi (up to 44%), Az (up to 22%), Pi+Az (up to 61%)], and H2O2 [Pi (up to 45%), Az (up to 28%), Pi+Az up to 57%)]. It was unveiled that the enhancement in activities of enzymatic and non-enzymatic antioxidants is probably the main mechanism underlying salt tolerance in microbial treated plants. During salt stress, dual inoculation of Pi and Az resulted an enhanced activities of antioxidant enzyme (superoxide dismutase, catalase, ascorbate peroxidase and glutathione reductase) and non-enzymatic antioxidants (total flavonoids, phenolics and carotenoids). Also, increase in artemisinin (56–64%) and proline (82–88%) content was recorded in co-inoculated plants (Pi+Az). These findings demonstrated the potentiality of Pi and Az dual symbiosis act as bio-ameliorator under saline conditions. This tripartite plant-microbial relationship could be a promising practice to alleviate the negative impact of salt stress on the productivity of medicinal plants.

Transcriptome analysis of soybean (Glycine max) root genes differentially expressed in rhizobial, arbuscular mycorrhizal, and dual symbiosis.

Soybean (Glycine max) roots establish associations with nodule-inducing rhizobia and arbuscular mycorrhizal (AM) fungi. Both rhizobia and AM fungi have been shown to affect the activity of and colonization by the other, and their interactions can be detected within host plants. Here, we report the transcription profiles of genes differentially expressed in soybean roots in the presence of rhizobial, AM, or rhizobial-AM dual symbiosis, compared with those in control (uninoculated) roots. Following inoculation, soybean plants were grown in a glasshouse for 6weeks; thereafter their root transcriptomes were analyzed using an oligo DNA microarray. Among the four treatments, the root nodule number and host plant growth were highest in plants with dual symbiosis. We observed that the expression of 187, 441, and 548 host genes was up-regulated and 119, 1,439, and 1,298 host genes were down-regulated during rhizobial, AM, and dual symbiosis, respectively. The expression of 34 host genes was up-regulated in each of the three symbioses. These 34 genes encoded several membrane transporters, type 1 metallothionein, and transcription factors in the MYB and bHLH families. We identified 56 host genes that were specifically up-regulated during dual symbiosis. These genes encoded several nodulin proteins, phenylpropanoid metabolism-related proteins, and carbonic anhydrase. The nodulin genes up-regulated by the AM fungal colonization probably led to the observed increases in root nodule number and host plant growth. Some other nodulin genes were down-regulated specifically during AM symbiosis. Based on the results above, we suggest that the contribution of AM fungal colonization is crucial to biological N2-fixation and host growth in soybean with rhizobial-AM dual symbiosis.

Match and mismatch between dietary switches and microbial partners in plant sap-feeding insects.

Some animal groups associate with the same vertically transmitted microbial symbionts over extended periods of evolutionary time, punctuated by occasional symbiont switches to different microbial taxa. Here we test the oft-repeated suggestion that symbiont switches are linked with host diet changes, focusing on hemipteran insects of the suborder Auchenorrhyncha. These insects include the only animals that feed on plant xylem sap through the life cycle, as well as taxa that feed on phloem sap and plant parenchyma cells. Ancestral state reconstruction provides strong statistical support for a xylem feeding auchenorrhynchan ancestor bearing the dual symbiosis with the primary symbiont Sulcia (Bacteroidetes) and companion symbiont 'β-Sym' (β-proteobacteria). We identified seven dietary transitions from xylem feeding (six to phloem feeding, one to parenchyma feeding), but no reversions to xylem feeding; five evolutionary losses of Sulcia, including replacements by yeast symbionts, exclusively in phloem/parenchyma-feeding lineages; and 14-15 losses of β-Sym, including nine transitions to a different bacterial companion symbiont. Our analysis indicates that, although companion symbiont switching is not associated with shifts in host diet, Sulcia is probably required for xylem-feeding. Furthermore, the ancestral auchenorrhynchan bearing Sulcia and β-Sym probably represents the sole evolutionary origin of xylem feeding in the animal kingdom.

The remediation of drought stress under VAM inoculation through proline chemical transformation action

This article discussed the enhanced drought tolerance under arbuscular mycorrhizal (AM) inoculation and normal growth of plants which linked with the activity of photoreceptors. The photoreceptor action in dual symbiosis under drought stress showed not only the high photosynthetic activity but also provide information about the broad range of physiological responses. The pot experiment conducted in a natural environment where drought condition was observed twice a week via regular irrigation with water up to twelve months. Plants analysis showed the high contents of water, hydrogen peroxide, carotenoids, proline, antioxidant enzymes like super dismutase (SOD) and catalase(CAT) in both leaves and roots with a large surface area of leaves over control. The elevated concentration of hydrogen peroxide (0.04 ± 0.0 μmol/g) coupled with singlet oxygen species was the main modified molecular mechanism which was operative in drought condition. The accretion of proline under drought stress in dual symbiosis (32.3 ± 0.3 μg/mL) was related to the highest branching pattern of young leaves and the chemical transformation of reactive oxygen species (ROS) including H2O2 and 3O2 into useful molecules like water and triplet molecular oxygen. The higher contents of carotenoids (5.0 ± 1.2 mg/g) in drought over control (4.8 ± 1.6 mg/g) and AM plant (4.9 ± 1.2 mg/g) was found to be supportive in the conversion of singlet oxygen into triplet one.

Didymella pinodes Affects N and P Uptakes and Their Efficiencies in a Tripartite Mutualism of Pea

In pea (Pisum sativum L.) production, Didymella pinodes (Berk. & A. Bloxam) Petr. is the most damaging aerial pathogen globally. In two completely randomized pot experiments with four replicates, we studied the effects of D. pinodes infection interaction with three symbiotic treatments (Rhizobium leguminosarum biovar viciae, arbuscular mycorrhizal fungi (AMF) and co-inoculation of both) and a non-symbiotic control on one or two pea cultivars. Grain yield and yield components of pea, uptakes and physiological efficiencies of N and P and nitrogen fixation were recorded. The results show that there were significant interaction effects among treatments. Therefore, productivity of crops and their uptakes and efficiencies of N and P are dependent on plant health conditions, effectiveness of microbial symbionts and response of pea genotypes. For cv. Protecta inoculated with both symbionts, pathogen infection compared to healthy plants significantly enhanced P acquisition. Overall, plants inoculated with rhizobia alone had higher grain yield by 20–30% and nitrogen fixation by 20–25% than in dual symbiosis independent of plant health conditions. In conclusion, aerial pathogen, pea genotypes and microbial symbionts interactions modified N and P uptake and their efficiencies, which can lead to improving final grain yield quantity and quality in a sustainable farming system.

Plasticity in root symbioses following shifts in soil nutrient availability during long‐term ecosystem development

Abstract The vast majority of terrestrial plants form root symbioses with arbuscular mycorrhizal (AM) fungi to enhance nutrient (particularly phosphorus, P) acquisition. However, some plant species also form dual symbioses involving ectomycorrhizal (ECM) fungi, with a subset of those also forming triple symbioses also involving dinitrogen (N2)‐fixing bacteria. It has been suggested that these plants show plasticity in root symbioses to optimise nutrient acquisition depending on the type and strength of soil nutrient limitation (e.g., N vs. P), yet empirical evidence remains limited. Alternatively, the degree of investment or “preference” in particular root symbioses might simply reflect differences in inoculum potential among soils of contrasting nutrient availability, reflecting adaptations of root symbionts to different edaphic conditions. Here, we grew two co‐occurring plant species forming triple (AM/ECM/N2‐fixing; Acacia rostellifera) or dual (AM/ECM; Melaleuca systena) symbioses in soils of increasing age and contrasting nutrient availability from an Australian long‐term soil chronosequence to disentangle the relative importance of abiotic factors (e.g., soil nutrient availability and stoichiometry) and biotic factors (e.g., soil inoculum potential) in determining root colonisation patterns and functional outcomes of these multiple root symbioses. For both plant species, we found clear hump‐shaped plant growth patterns along the pedogenesis‐driven gradient in soil nutrient availability, with peak growth in intermediate‐aged soils, while high levels of mycorrhizal colonisation by the “preferred” root symbionts were maintained across all soils. We found large increases (540%) in foliar manganese concentrations with increasing soil age and declining P availability, suggesting that plants may be relying on the release of carboxylates to help acquire P in the most P‐impoverished soils. Finally, we found that soil abiotic properties, such as strong differences in soil nutrient availability, are generally more important than soil inoculum potential in explaining these shifts in our plant and root responses. Synthesis. Our study suggests that plants capable of forming multiple root symbioses show plasticity in their nutrient‐acquisition strategies following shifts in soil nutrients during long‐term ecosystem development, yet maintain a preference for certain root symbionts despite changes in soil microbial inoculum.

New Prospective for Enhancement in Bioenergy Resources Through Fungal Engineering.

Lignin and cellulose, organic constituents of the plant or plant-based material not commonly used for feeding purpose are referred as Biomass. Patents suggest that this can be used as the best resource of renewable energy. Vesicular Arbuscular Mycorrhizae (VAM) fungi can play an effective role in biomass manufacturing through activated metabolism of the plant under dual symbiosis. During C acclimatization, mycorrhizal inoculated plants existent greater number of leaves with a height of plants as compared to non-mycorrhizal plants. The current article discloses the search of the natural resources for C assimilation into biomass using mycorrhizal symbiosis. The pot experiment was conducted in the natural environment for extraction of more bioenergy through biomass of Conocarpus erectus L under VAM (Glomus fasciculatum) inoculation in various environmental conditions with replicates. It observed that these fungal engineered plants showed distinctive prospective to offer, enhanced biomass to energy couple with a strong network for sinking CO2 from the atmosphere via strong roots and large surface area of leaves. There was an increase in biomass (9-17% respectively) of the plant under drought-VAM, VAM inoculation and VAM- enriched CO2 conditions in same period in comparison to control plants through lignin, cellulose and carbohydrate contents. It was followed by enhanced enzyme activities and nutrient ions in dual symbiosis. Coupling biomass-originated energy may recover environmental conditions and commercial value for sustainable growth in energy consumption sector. The green energy from fungal engineered plants may replace high demand of fossil fuel as a young biofuel and make the cities more productive in the fabrication of bioenergy too in the form of biomass or biofuel with C impartial atmosphere.

Improvement of cowpea productivity by rhizobial and mycorrhizal inoculation in Burkina Faso

Cowpea is one of the most important food legume crops in Burkina Faso. It is able to associate with arbuscular mycorrhizal fungi (AMF) and rhizobia. This dual symbiosis improves nitrogen and phosphorus nutrient uptake in cowpea. As the application of exotic inoculants frequently lacks positive responses in field experiments, this study set out to select well-adapted native symbiotic rhizobial and AMF strains. Soil samples were collected from six study sites in three different climatic zones of Burkina Faso to investigate their native symbiotic strains. Soil-extraction of native spores led to the identification of four AMF genera (Scutellospora, Gigaspora, Glomus and Entrophospora) by morpho-anatomical characterization. The two most effective cowpea fungal strains were selected after spore isolation from field-collected soils, multiplication on maize roots and inoculation on cowpea seedlings in a greenhouse experiment. Cowpea-nodulating rhizobial strains were trapped in the greenhouse by planting cowpea seeds in collected soil samples and the strains were characterized using molecular methods. This characterization led to the rhizobial isolates being classified in four clusters on the phylogenetic tree (using the Maximum-Likelihood Phylogenies method). All strains belonged to the Bradyrhizobium genus and most of them were included in the B. japonicum branch. Some groups were clearly distinct species already identified and may be new species. The two most effective strains for cowpea yield improvement in the field were selected after cowpea inoculation in a greenhouse experiment. The inoculation design in the field experiment consisted of four single inoculation treatments, either rhizobial or mycorrhizal, along with four dual inoculations, one treatment with chemical fertilizers, and one uninoculated control. The results showed that cowpea productivity was significatively improved by dual inoculation with native rhizobial and mycorrhizal strains, reaching the same level as the application of commonly used chemical fertilizers [Nitrogen, Phosphorus and Potassium fertilizers (NPK)]. In addition, dual inoculation resulted in the highest iron content in cowpea leaves.

Colwellia and sulfur-oxidizing bacteria: An unusual dual symbiosis in a Terua mussel (Mytilidae: Bathymodiolinae) from whale falls in the Antilles arc

Seven individuals of a single morphotype of mussels (Bivalvia: Mytilidae) were found attached to a naturally sunken whale intervertebral disk collected in Guadeloupe (Caribbean) at 800m depth. These specimens resemble small Idas mussels which are found worldwide at cold seeps and hydrothermal vents, and typically harbor ectosymbiotic bacteria on their gills upon which they depend for nutrition. Based on multi-locus gene sequencing, these specimens appear to belong to a new species closely related to two species now included within the genus Terua. Unexpectedly, its closest relatives are found in the Pacific, questioning how this species has reached the Antilles arc. Based on marker gene sequence analysis, electron and fluorescence microscopy, Terua n. sp. harbors two distinct and abundant extracellular bacterial symbionts located between microvilli at the apical surface of host gill epithelial cells. One is a sulfur-oxidizing bacterium similar to the symbionts previously identified in several deep-sea mussels, while the other is related to Colwellia species, a group of cold-adapted heterotrophic bacteria able to degrade organic compounds. This study provides the first evidence for the existence of a dual symbiosis in mussels from whale fall ecosystems in the Caribbean. The evolutionary history of Terua n. sp. and potential role of its Colwellia symbionts are discussed.

Glomus fasciculatum Fungi as a Bio-convertor and Bio-activator of Inorganic and Organic P in Dual Symbiosis.

Dual symbiosis played an effective role in drought condition and temperature. Furthermore, performed services in absorption of water and solubilization of chief nutrients specially phosphorus for growth of plants. Phosphorous is essential for plant growth in any climatic condition because of central constituent of ATP providing chemical energy for all metabolic reactions of plants. The goal of this work was to monitor the growth of plant under three climatic conditions in comparison to control plant under Glomus fasciculatum inoculation related with adequate supply of phosphorous. Results demonstrated that Glomus fasciculatum (VAM) activates the solubilization of P into the anionic form H2PO4(-) which is highly consumable form by the plants. Minerals including P in soil most regularly solubilized for fixing in plants and continuously changed to highly soluble forms by reaction with inorganic or organic constituents of the soil which are activated in the presence of fungi for continuous availability. Experimental facts and nonstop growth of plants recommended that VAM fungi act as a bio-convertor and bio-activator of soil nutrients, especially of P and their hyphal interaction absorbs soil nutrients and activates insoluble P to soluble one for plant development. Continuous growth of 18 months old Conocarpus erectus L plant in dual symbiosis supports the proposed idea that phosphorus cycle exists during VAM inoculations, where soil reaction altered in presence of spores that help to solubilize the P which strengthens the plant, activates photo-biological activity and demonstrates the new function of VAM as a recycler for continues growth.

Shifts in symbiotic associations in plants capable of forming multiple root symbioses across a long-term soil chronosequence.

Changes in soil nutrient availability during long‐term ecosystem development influence the relative abundances of plant species with different nutrient‐acquisition strategies. These changes in strategies are observed at the community level, but whether they also occur within individual species remains unknown. Plant species forming multiple root symbioses with arbuscular mycorrhizal (AM) fungi, ectomycorrhizal (ECM) fungi, and nitrogen‐(N) fixing microorganisms provide valuable model systems to examine edaphic controls on symbioses related to nutrient acquisition, while simultaneously controlling for plant host identity. We grew two co‐occurring species, Acacia rostellifera (N2‐fixing and dual AM and ECM symbioses) and Melaleuca systena (AM and ECM dual symbioses), in three soils of contrasting ages (c. 0.1, 1, and 120 ka) collected along a long‐term dune chronosequence in southwestern Australia. The soils differ in the type and strength of nutrient limitation, with primary productivity being limited by N (0.1 ka), co‐limited by N and phosphorus (P) (1 ka), and by P (120 ka). We hypothesized that (i) within‐species root colonization shifts from AM to ECM with increasing soil age, and that (ii) nodulation declines with increasing soil age, reflecting the shift from N to P limitation along the chronosequence. In both species, we observed a shift from AM to ECM root colonization with increasing soil age. In addition, nodulation in A. rostellifera declined with increasing soil age, consistent with a shift from N to P limitation. Shifts from AM to ECM root colonization reflect strengthening P limitation and an increasing proportion of total soil P in organic forms in older soils. This might occur because ECM fungi can access organic P via extracellular phosphatases, while AM fungi do not use organic P. Our results show that plants can shift their resource allocation to different root symbionts depending on nutrient availability during ecosystem development.

Understanding Microbial Multi-Species Symbioses.

Lichens are commonly recognized as a symbiotic association of a fungus and a chlorophyll containing partner, either green algae or cyanobacteria, or both. The fungus provides a suitable habitat for the partner, which provides photosynthetically fixed carbon as energy source for the system. The evolutionary result of the self-sustaining partnership is a unique joint structure, the lichen thallus, which is indispensable for fungal sexual reproduction. The classical view of a dual symbiosis has been challenged by recent microbiome research, which revealed host-specific bacterial microbiomes. The recent results about bacterial associations with lichens symbioses corroborate their notion as a multi-species symbiosis. Multi-omics approaches have provided evidence for functional contribution by the bacterial microbiome to the entire lichen meta-organism while various abiotic and biotic factors can additionally influence the bacterial community structure. Results of current research also suggest that neighboring ecological niches influence the composition of the lichen bacterial microbiome. Specificity and functions are here reviewed based on these recent findings, converging to a holistic view of bacterial roles in lichens. Finally we propose that the lichen thallus has also evolved to function as a smart harvester of bacterial symbionts. We suggest that lichens represent an ideal model to study multi-species symbiosis, using the recently available omics tools and other cutting edge methods.

Estimating Symbiont Abundances and Gill Surface Areas in Specimens of the Hydrothermal Vent Mussel Bathymodiolus puteoserpentis Maintained in Pressure Vessels

The hydrothermal vent mussel Bathymodiolus puteoserpentis hosts gill-associated sulfur- and methane-oxidizing bacteria which sustain host nutrition and allow it to reach high densities at various sites along the northern Mid-Atlantic Ridge. Previous studies have demonstrated that in similar dual symbioses, relative abundances of each bacterial type could change following variations in symbiont substrate availabilities. In this study, pressurized recovery and incubations in pressure vessels were used to test whether B. puteoserpentis symbionts displayed similar behavior in the presence of symbiont substrates. The relative abundances of both types of symbionts were analyzed using fluorescence in situ hybridization (FISH) and group-specific gene copy numbers were assessed using qPCR. Specimens sampled using isobaric and non-isobaric recovery contained similar relative proportions (in surface coverage) of sulfur- and methane-oxidizing bacteria indicating that recovery type did not have impact on measured relative areas. Similarly, pressurized incubations with different substrates did lead to significant differences in the relative surface coverage of the two types of bacteria, although slight variations were measured with qPCR, suggesting changes in relative abundances of gene copy numbers but not in relative areas covered. Total gill surface areas and total bacterial numbers in specimens were estimated for the first time. Symbiont bearing-mussels display exchange surfaces about 20-fold higher than those found in similar-sized coastal mussels, and mean bacterial numbers of 2.5*1012 per specimen were estimated. This emphasizes that symbiotic mussels are a major reservoir of bacteria in vent ecosystems.

Glomus Fasciculatum Fungi as a Bio-Convertor and Bio-Activator of Inorganic and Organic P in Dual Symbiosis

Glomus Fasciculatum Fungi as a Bio-Convertor and Bio-Activator of Inorganic and Organic P in Dual Symbiosis

Functional analysis of liverworts in dual symbiosis with Glomeromycota and Mucoromycotina fungi under a simulated Palaeozoic CO2 decline.

Most land plants form mutualistic associations with arbuscular mycorrhizal fungi of the Glomeromycota, but recent studies have found that ancient plant lineages form mutualisms with Mucoromycotina fungi. Simultaneous associations with both fungal lineages have now been found in some plants, necessitating studies to understand the functional and evolutionary significance of these tripartite associations for the first time. We investigate the physiology and cytology of dual fungal symbioses in the early-diverging liverworts Allisonia and Neohodgsonia at modern and Palaeozoic-like elevated atmospheric CO2 concentrations under which they are thought to have evolved. We found enhanced carbon cost to liverworts with simultaneous Mucoromycotina and Glomeromycota associations, greater nutrient gain compared with those symbiotic with only one fungal group in previous experiments and contrasting responses to atmospheric CO2 among liverwort–fungal symbioses. In liverwort–Mucoromycotina symbioses, there is increased P-for-C and N-for-C exchange efficiency at 440 p.p.m. compared with 1500 p.p.m. CO2. In liverwort–Glomeromycota symbioses, P-for-C exchange is lower at ambient CO2 compared with elevated CO2. No characteristic cytologies of dual symbiosis were identified. We provide evidence of a distinct physiological niche for plant symbioses with Mucoromycotina fungi, giving novel insight into why dual symbioses with Mucoromycotina and Glomeromycota fungi persist to the present day.