Dataset Information

Nutrient Dependent Cross-Kingdom Interactions: Fungi and Bacteria From an Oligotrophic Desert Oasis.

ABSTRACT: Microbial interactions play a key role in ecosystem functioning, with nutrient availability as an important determinant. Although phylogenetically distant bacteria and fungi commonly co-occur in nature, information on their cross-kingdom interactions under unstable, extreme environments remains poor. Hence, the aims of this work were to evaluate potential in vitro interactions among fungi and bacteria isolated from a phosphorous oligotrophic aquatic system in the Cuatro Ciénegas Basin, Mexico, and to test the nutrients-based shifts. We assessed growth changes in bacteria (Aeromonas and Vibrio) and fungi (Coprinellus micaceus, Cladosporium sp., and Aspergillus niger) on co-cultures in relation to monocultures under diverse nutrient scenarios on Petri dishes. Interactions were explored using a network analysis, and a metabolome profiling for specific taxa. We identified nutrient-dependent patterns, as beneficial interactions dominated in low-nutrients media and antagonistic interactions dominated in rich media. This suggests that cross-kingdom synergistic interactions might favor microbial colonization and growth under low nutrient conditions, representing an adaptive trait to oligotrophic environments. Moreover, our findings agree with the stress-gradient hypothesis, since microbial interactions shifted from competition to cooperation as environmental stress (expressed as low nutrients) increased. At a functional level consistent differences were detected in the production of secondary metabolites, agreeing with plate bioassays. Our results based on culture experiments, provides evidence to understand the complexity of microbial dynamics and survival in phosphorous-depleted environments.

SUBMITTER: Velez P

PROVIDER: S-EPMC6090137 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Nutrient Dependent Cross-Kingdom Interactions: Fungi and Bacteria From an Oligotrophic Desert Oasis.

Velez Patricia P Espinosa-Asuar Laura L Figueroa Mario M Gasca-Pineda Jaime J Aguirre-von-Wobeser Eneas E Eguiarte Luis E LE Hernandez-Monroy Abril A Souza Valeria V

Frontiers in microbiology 20180806

Microbial interactions play a key role in ecosystem functioning, with nutrient availability as an important determinant. Although phylogenetically distant bacteria and fungi commonly co-occur in nature, information on their cross-kingdom interactions under unstable, extreme environments remains poor. Hence, the aims of this work were to evaluate potential <i>in vitro</i> interactions among fungi and bacteria isolated from a phosphorous oligotrophic aquatic system in the Cuatro Ciénegas Basin, Me ...[more]

PMID: 30131780

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Project description:IntroductionThe hyphosphere of arbuscular mycorrhizal (AM) fungi is teeming with microbial life. Yet, the influence of nutrient availability or nutrient forms on the hyphosphere microbiomes is still poorly understood.MethodsHere, we examined how the microbial community (prokaryotic, fungal, protistan) was affected by the presence of the AM fungus Rhizophagus irregularis in the rhizosphere and the root-free zone, and how different nitrogen (N) and phosphorus (P) supplements into the root-free compartment influenced the communities.ResultsThe presence of AM fungus greatly affected microbial communities both in the rhizosphere and the root-free zone, with prokaryotic communities being affected the most. Protists were the only group of microbes whose richness and diversity were significantly reduced by the presence of the AM fungus. Our results showed that the type of nutrients AM fungi encounter in localized patches modulate the structure of hyphosphere microbial communities. In contrast we did not observe any effects of the AM fungus on (non-mycorrhizal) fungal community composition. Compared to the non-mycorrhizal control, the root-free zone with the AM fungus (i.e., the AM fungal hyphosphere) was enriched with Alphaproteobacteria, some micropredatory and copiotroph bacterial taxa (e.g., Xanthomonadaceae and Bacteroidota), and the poorly characterized and not yet cultured Acidobacteriota subgroup GP17, especially when phytate was added. Ammonia-oxidizing Nitrosomonas and nitrite-oxidizing Nitrospira were significantly suppressed in the presence of the AM fungus in the root-free compartment, especially upon addition of inorganic N. Co-occurrence network analyses revealed that microbial communities in the root-free compartment were complex and interconnected with more keystone species when AM fungus was present, especially when the root-free compartment was amended with phytate.ConclusionOur study showed that the form of nutrients is an important driver of prokaryotic and eukaryotic community assembly in the AM fungal hyphosphere, despite the assumed presence of a stable and specific AM fungal hyphoplane microbiome. Predictable responses of specific microbial taxa will open the possibility of using them as co-inoculants with AM fungi, e.g., to improve crop performance.

Project description:The phylum Actinobacteria constitutes one of the largest and anciently divergent phyla within the Bacteria domain. Actinobacterial diversity has been thoroughly researched in various environments due to its unique biotechnological potential. Such studies have focused mostly on soil communities, but more recently marine and extreme environments have also been explored, finding rare taxa and demonstrating dispersal limitation and biogeographic patterns for Streptomyces. To test the distribution of Actinobacteria populations on a small scale, we chose the extremely oligotrophic and biodiverse Cuatro Cienegas Basin (CCB), an endangered oasis in the Chihuahuan desert to assess the diversity and uniqueness of Actinobacteria in the Churince System with a culture-dependent approach over a period of three years, using nine selective media. The 16S rDNA of putative Actinobacteria were sequenced using both bacteria universal and phylum-specific primer pairs. Phylogenetic reconstructions were performed to analyze OTUs clustering and taxonomic identification of the isolates in an evolutionary context, using validated type species of Streptomyces from previously phylogenies as a reference. Rarefaction analysis for total Actinobacteria and for Streptomyces isolates were performed to estimate species' richness in the intermediate lagoon (IL) in the oligotrophic Churince system. A total of 350 morphologically and nutritionally diverse isolates were successfully cultured and characterized as members of the Phylum Actinobacteria. A total of 105 from the total isolates were successfully subcultured, processed for DNA extraction and 16S-rDNA sequenced. All strains belong to the order Actinomycetales, encompassing 11 genera of Actinobacteria; the genus Streptomyces was found to be the most abundant taxa in all the media tested throughout the 3-year sampling period. Phylogenetic analysis of our isolates and another 667 reference strains of the family Streptomycetaceae shows that our isolation effort produced 38 unique OTUs in six new monophyletic clades. This high biodiversity and uniqueness of Actinobacteria in an extreme oligotrophic environment, which has previously been reported for its diversity and endemicity, is a suggestive sign of microbial biogeography of Actinobacteria and it also represents an invaluable source of biological material for future ecological and bioprospecting studies.

Project description:The Cuatro Ciénegas Basin (CCB) comprises several oligotrophic aquatic ecosystems limited by phosphorus. These aquatic systems are dominated by a high prokaryotic diversity, shaped by the stress of low nutrient supplies and interspecific competition. Although fungi constitute a diverse and important component of microbial diversity, the microfungal diversity in the CCB remains to be unveiled. With the aim to explore microfungal diversity and ecological patterns in this area, we present the first investigation analyzing cultivable taxa from sediment and water, as well as lignocellulolytic taxa obtained from incubated submerged plant debris, and wood panels in three contrasting freshwater systems in the CCB: Churince, Becerra and Pozas Rojas. We chose a culture-based approach to analyze sediment and water samples in order to obtain fungal cultures, providing opportunities for a posteriori studies, and the possibility of ex situ preservation of the diversity. We evaluated sequence data from the nuclear ribosomal internal transcribed spacer including the 5.8 rDNA region for 126 isolates, revealing 37 OTUs. These OTUs were phylogenetically affiliated to several genera in the fungal phyla: Zygomycota, Basidiomycota, and Ascomycota. We recorded two OTUs with saline affinity, agreeing with previous findings on the prokaryotic communities with ancestral marine resemblances. All the studied systems showed moderate diversity levels, however discrepancies among the diversity indexes were observed, due to the occurrence of abundant taxa in the samples. Our results indicated that lignocellulolytic microfungal communities are dominated by transient fungal taxa, as resident species were not recorded perhaps as a result of the long-term strong competition with the highly adapted prokaryotic community. Moreover, the obtained microfungal taxa occurred mostly on the resident plant debris, rather than submerged wood panels, perhaps as a result of the high adaptation to specific environmental conditions. In conclusion, the CCB possess a moderate taxonomical diversity compared to other arid environments, probably as a result of high selective pressures. Nonetheless, due to high spatial and temporal heterogeneity, the functional fungal diversity was considerable as predicted by the intermediate disturbance hypothesis. Decisively, the assessment of microfungal diversity freshwater systems is relevant, since this ecological group of microorganisms represents an important indicator of trophic complexity and biotic interactions among microbial communities, having important implications for understanding eukaryotic survival at the oligotrophic limit for life.

Project description:Reptiles and amphibians (herptiles) are some of the most endangered and threatened species on the planet and numerous conservation strategies are being implemented with the goal of ensuring species recovery. Little is known, however, about the gut microbiome of wild herptiles and how it relates to the health of these populations. Here, we report results from the gut microbiome characterization of both a broad survey of herptiles, and the correlation between the fungus Basidiobolus, and the bacterial community supported by a deeper, more intensive sampling of Plethodon glutinosus, known as slimy salamanders. We demonstrate that bacterial communities sampled from frogs, lizards, and salamanders are structured by the host taxonomy and that Basidiobolus is a common and natural component of these wild gut microbiomes. Intensive sampling of multiple hosts across the ecoregions of Tennessee revealed that geography and host:geography interactions are strong predictors of distinct Basidiobolus operational taxonomic units present within a given host. Co-occurrence analyses of Basidiobolus and bacterial community diversity support a correlation and interaction between Basidiobolus and bacteria, suggesting that Basidiobolus may play a role in structuring the bacterial community. We further the hypothesis that this interaction is advanced by unique specialized metabolism originating from horizontal gene transfer from bacteria to Basidiobolus and demonstrate that Basidiobolus is capable of producing a diversity of specialized metabolites including small cyclic peptides.IMPORTANCEThis work significantly advances our understanding of biodiversity and microbial interactions in herptile microbiomes, the role that fungi play as a structural and functional members of herptile gut microbiomes, and the chemical functions that structure microbiome phenotypes. We also provide an important observational system of how the gut microbiome represents a unique environment that selects for novel metabolic functions through horizontal gene transfer between fungi and bacteria. Such studies are needed to better understand the complexity of gut microbiomes in nature and will inform conservation strategies for threatened species of herpetofauna.

Project description:BackgroundLinking the identity of wild microbes with their ecophysiological traits and environmental functions is a key ambition for microbial ecologists. Of many techniques that strive for this goal, Stable-isotope probing-SIP-remains among the most comprehensive for studying whole microbial communities in situ. In DNA-SIP, actively growing microorganisms that take up an isotopically heavy substrate build heavier DNA, which can be partitioned by density into multiple fractions and sequenced. However, SIP is relatively low throughput and requires significant hands-on labor. We designed and tested a semi-automated, high-throughput SIP (HT-SIP) pipeline to support well-replicated, temporally resolved amplicon and metagenomics experiments. We applied this pipeline to a soil microhabitat with significant ecological importance-the hyphosphere zone surrounding arbuscular mycorrhizal fungal (AMF) hyphae. AMF form symbiotic relationships with most plant species and play key roles in terrestrial nutrient and carbon cycling.ResultsOur HT-SIP pipeline for fractionation, cleanup, and nucleic acid quantification of density gradients requires one-sixth of the hands-on labor compared to manual SIP and allows 16 samples to be processed simultaneously. Automated density fractionation increased the reproducibility of SIP gradients compared to manual fractionation, and we show adding a non-ionic detergent to the gradient buffer improved SIP DNA recovery. We applied HT-SIP to 13C-AMF hyphosphere DNA from a 13CO2 plant labeling study and created metagenome-assembled genomes (MAGs) using high-resolution SIP metagenomics (14 metagenomes per gradient). SIP confirmed the AMF Rhizophagus intraradices and associated MAGs were highly enriched (10-33 atom% 13C), even though the soils' overall enrichment was low (1.8 atom% 13C). We assembled 212 13C-hyphosphere MAGs; the hyphosphere taxa that assimilated the most AMF-derived 13C were from the phyla Myxococcota, Fibrobacterota, Verrucomicrobiota, and the ammonia-oxidizing archaeon genus Nitrososphaera.ConclusionsOur semi-automated HT-SIP approach decreases operator time and improves reproducibility by targeting the most labor-intensive steps of SIP-fraction collection and cleanup. We illustrate this approach in a unique and understudied soil microhabitat-generating MAGs of actively growing microbes living in the AMF hyphosphere (without plant roots). The MAGs' phylogenetic composition and gene content suggest predation, decomposition, and ammonia oxidation may be key processes in hyphosphere nutrient cycling. Video Abstract.

Dataset Information

Nutrient Dependent Cross-Kingdom Interactions: Fungi and Bacteria From an Oligotrophic Desert Oasis.

Publications

Nutrient Dependent Cross-Kingdom Interactions: Fungi and Bacteria From an Oligotrophic Desert Oasis.

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