One promise of the recently presented microbiome definition suggested that, in combination with unifying concepts and standards, microbiome research could be important for solving new challenges ...associated with anthropogenic-driven changes in various microbiota. With this commentary we want to further elaborate this suggestion, because we noticed specific signatures in microbiota affected by the Anthropocene.
Here, we discuss this based on a review of available literature and our own research targeting exemplarily the plant microbiome. It is not only crucial for plants themselves but also linked to planetary health. We suggest that different human activities are commonly linked to a shift of diversity and evenness of the plant microbiota, which is also characterized by a decrease of host specificity, and an increase of r-strategic microbes, pathogens, and hypermutators. The resistome, anchored in the microbiome, follows this shift by an increase of specific antimicrobial resistance (AMR) mechanisms as well as an increase of plasmid-associated resistance genes. This typical microbiome signature of the Anthropocene is often associated with dysbiosis and loss of resilience, and leads to frequent pathogen outbreaks. Although several of these observations are already confirmed by meta-studies, this issue requires more attention in upcoming microbiome studies.
Our commentary aims to inspire holistic studies for the development of solutions to restore and save microbial diversity for ecosystem functioning as well as the closely connected planetary health. Video abstract.
Cereal crop production is severely affected by seed-borne bacterial diseases across the world. Locally occurring disease resistance in various crops remains elusive. Here, we have observed that rice ...plants of the same cultivar can be differentiated into disease-resistant and susceptible phenotypes under the same pathogen pressure. Following the identification of a seed-endophytic bacterium as the resistance-conferring agent, integration of high-throughput data, gene mutagenesis and molecular interaction assays facilitated the discovery of the underlying mode of action. Sphingomonas melonis that is accumulated and transmitted across generations in disease-resistant rice seeds confers resistance to disease-susceptible phenotypes by producing anthranilic acid. Without affecting cell growth, anthranilic acid interferes with the sigma factor RpoS of the seed-borne pathogen Burkholderia plantarii, probably leading to impairment of upstream cascades that are required for virulence factor biosynthesis. The overall findings highlight the hidden role of seed endophytes in the phytopathology paradigm of 'disease triangles', which encompass the plant, pathogens and environmental conditions. These insights are potentially exploitable for modern crop cultivation threatened by globally widespread bacterial diseases.
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GEOZS, IJS, IMTLJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBMB, UL, UM, UPUK, ZAGLJ
Mutualistic interactions within microbial assemblages provide a survival strategy under extreme conditions; however, little is known about the complexity of interaction networks in multipartite, ...free-living communities. In the present study, the interplay within algae-dominated microbial communities exposed to harsh environmental influences in the Austrian Alps was assessed in order to reveal the interconnectivity of eukaryotic and prokaryotic inhabitants. All analyzed snowfields harbored distinct microbial communities. Network analyses revealed that mutual exclusion prevailed among microalgae in the alpine environment, while bacteria were mainly positively embedded in the interaction networks. Especially members of Proteobacteria, with a high prevalence of Oxalobacteraceae, Pseudomonadaceae, and Sphingomonadaceae showed genus-specific co-occurrences with distinct microalgae. Co-cultivation experiments with algal and bacterial isolates confirmed beneficial interactions that were predicted based on the bioinformatic analyses; they resulted in up to 2.6-fold more biomass for the industrially relevant microalga Chlorella vulgaris, and up to 4.6-fold increase in biomass for the cryophilic Chloromonas typhlos. Our findings support the initial hypothesis that microbial communities exposed to adverse environmental conditions in alpine systems harbor inter-kingdom supportive capacities. The insights into mutualistic inter-kingdom interactions and the ecology of microalgae within complex microbial communities provide explanations for the prevalence and resilience of such assemblages in alpine environments.
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NUK, SBMB, SBNM, UL, UM, UPUK
Plant-associated microorganisms are involved in important functions related to growth, performance and health of their hosts. Understanding their modes of action is important for the design of ...promising microbial inoculants for sustainable agriculture. Plant-associated microorganisms are able to interact with their hosts and often exert specific functions toward potential pathogens; the underlying
interactions are well studied. In contrast,
effects of inoculants, and especially their impact on the plant indigenous microbiome was mostly neglected so far. Recently, microbiome research has revolutionized our understanding of plants as coevolved holobionts but also of indigenous microbiome-inoculant interactions. Here we disentangle the effects of microbial inoculants on the indigenous plant microbiome and point out the following types of plant microbiome modulations: (i) transient microbiome shifts, (ii) stabilization or increase of microbial diversity, (iii) stabilization or increase of plant microbiome evenness, (iv) restoration of a dysbiosis/compensation or reduction of a pathogen-induced shift, (v) targeted shifts toward plant beneficial members of the indigenous microbiota, and (vi) suppression of potential pathogens. Therefore, we suggest microbiome modulations as novel and efficient mode of action for microbial inoculants that can also be mediated
the plant.
Recent studies have shown that various agrochemicals can substantially affect microbial communities; especially those that are associated with cultivated plants. Under certain circumstances, up to ...50% of the naturally occurring microorganisms can be negatively affected by common agricultural practices such as seed coating with fungicide-based matrices. Nevertheless, the off-target effects of commonly applied agrochemicals are still understudied in terms of their interferences with microbial communities. At the same time, agrochemical inputs are steadily increasing due to the intensification of agriculture and the increasing pathogen pressure that is currently observed worldwide. In this article, we briefly reflect on the current knowledge related to pesticide interference with microbial communities and discuss negative implications for the plant holobiont as well as such that are spanning beyond local system borders. Cumulative effects of pesticide inputs that cause alterations in microbial functioning likely have unforeseen implications on geochemical cycles that should be addressed with a high priority in ongoing research. A holistic assessment of such implications will allow us to objectively select the most suitable means for food production under the scenario of a growing global population and aggravating climatic conditions. We present three hypothetical solutions that might facilitate a more sustainable and less damaging application of pesticides in the future.
•Microbial communities are affected by off-target effects exerted by agrochemicals.•Shifts in microbial populations likely have substantial implications on biogeochemical fluxes.•Sustainable crop production must take plant-associated microbes into consideration.•Microbiota bioengineering can provide yet unexploited solutions.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Plant-associated microorganisms are known to contribute with various beneficial functions to the health and productivity of their hosts, yet the microbiome of most plants remains unexplored. This ...especially applies to wild relatives of cultivated plants, which might harbor beneficial microorganisms that were lost during intensive breeding. We studied bacterial communities of the Himalayan onion (
Allium wallichii
Kunth), a wild relative of onion native to mountains in East Asia. The bacterial community structure was assessed in different plant microhabitats (rhizosphere, endosphere, anthosphere) by sequencing of 16S rRNA gene fragment amplicons. Targeted bioinformatic analyses were implemented in order to identify unique features in each habitat and to map the overall community in the first representative of the Amaryllidaceae plant family. The highest bacterial diversity was found for bulk soil (Shannon index,
H
′ 9.3) at the high-altitude sampling location. It was followed by the plant rhizosphere (
H
′ 8.9) while communities colonizing flowers (
H
′ 6.1) and the endosphere (
H
′ 6.5 and 5.6) where less diverse. Interestingly, we observed a non-significant rhizosphere effect. Another specificity of the microbiome was its high evenness in taxonomic distribution, which was so far not observed in plant microbiomes.
Pseudomonas
was identified among additional 10 bacterial genera as a plant-specific signature. The first insights into the microbiome of a plant in the widespread
Allium
genus will facilitate upcoming comparisons with its domesticated relatives while additionally providing a detailed microbiome mapping of the plant’s microhabitats to facilitate bioresource mining.
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EMUNI, FZAB, GEOZS, IJS, IMTLJ, KILJ, KISLJ, MFDPS, NUK, OILJ, PNG, SAZU, SBCE, SBJE, SBMB, SBNM, UKNU, UL, UM, UPUK, VKSCE, ZAGLJ
Myzus persicae
(Sulzer) is an important insect pest in agriculture that has a very broad host range. Previous research has shown that the microbiota of insects has implications for their growth, ...development, and environmental adaptation. So far, there is little detailed knowledge about the factors that influence and shape the microbiota of aphids. In the present study, we aimed to investigate diet-induced changes in the microbiome of
M. persicae
using high-throughput sequencing of bacterial 16S ribosomal RNA gene fragments in combination with molecular and microbiological experiments. The transfer of aphids to different plants from the Solanaceae family resulted in a substantial decrease in the abundance of the primary symbiont
Buchnera
. In parallel, a substantial increase in the abundance of
Pseudomonas
was observed; it accounted for up to 69.4% of the bacterial community in
M. persicae
guts and the attached bacteriocytes. In addition, we observed negative effects on aphid population dynamics when they were transferred to pepper plants (
Capsicum annuum
L.). The microbiome of this treatment group showed a significantly lower increase in the abundance of
Pseudomonas
when compared with the other Solanaceae plant diets, which might be related to the adaptability of the host to this diet. Molecular quantifications of bacterial genera that were substantially affected by the different diets were implemented as an additional verification of the microbiome-based observations. Complementary experiments with bacteria isolated from aphids that were fed with different plants indicated that nicotine-tolerant strains occur in Solanaceae-fed specimens, but they were not restricted to them. Overall, our mechanistic approach conducted under controlled conditions provided strong indications that the aphid microbiome shows responses to different plant diets. This knowledge could be used in the future to develop environmentally friendly methods for the control of insect pests in agriculture.
Knowledge of bacterial community host‐specificity has increased greatly in recent years. However, the intermicrobiome relationships of unrelated but spatially close organisms remain little ...understood. Trunks of trees covered by epiphytes represent complex habitats with a mosaic of ecological niches. In this context, we investigated the structure, diversity and interactions of microbiota associated with lichens, mosses and the bare tree bark. Comparative analysis revealed significant differences in the habitat‐associated community structures. Corresponding co‐occurrence analysis indicated that the lichen microbial network is less complex and less densely interconnected than the moss‐ and bark‐associated networks. Several potential generalists and specialists were identified for the selected habitats. Generalists belonged mainly to Proteobacteria, with Sphingomonas as the most abundant genus. The generalists comprise microorganisms with generally beneficial features, such as nitrogen fixation or other supporting functions, according to a metagenomic analysis. We argue that beneficial strains shared among hosts contribute to ecological stability of the host biocoenoses.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
The plant microbiota is crucial for plant health and growth. Recently, vertical transmission of a beneficial core microbiota was identified for crop seeds, but for native plants, complementary ...mechanisms are almost completely unknown.
We studied the seeds of eight native plant species growing together for centuries under the same environmental conditions in Alpine meadows (Austria) by qPCR, FISH-CLSM, and amplicon sequencing targeting bacteria, archaea, and fungi.
Bacteria and fungi were determined with approx. 10
gene copy numbers g
seed as abundant inhabitants. Archaea, which were newly discovered as seed endophytes, are less and represent only 1.1% of the signatures. The seed microbiome was highly diversified, and all seeds showed a species-specific, highly unique microbial signature, sharing an exceptionally small core microbiome. The plant genotype (species) was clearly identified as the main driver, while different life cycles (annual/perennial) had less impact on the microbiota composition, and fruit morphology (capsule/achene) had no significant impact. A network analysis revealed significant co-occurrence patterns for bacteria and archaea, contrasting with an independent fungal network that was dominated by mutual exclusions.
These novel insights into the native seed microbiome contribute to a deeper understanding of seed microbial diversity and phytopathological processes for plant health, and beyond that for ecosystem plasticity and diversification within plant-specific microbiota.
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