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Institute
Background:
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.
Results:
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.
Conclusions:
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.
Microbiome science is revolutionizing many concepts of plant biology, ecology, and evolution.
Understanding plant microbiomes is key to developing solutions that protect crop health without impacting the environment.
In this perspective article, we highlight the importance of both the structure and functions of plant-associated microbial communities in protecting their host from pathogens.
These new findings have a high potential to aid biocontrol programs and to replace traditional chemical products, guiding the transition towards a sustainable production.
The production of volatile organic compounds (VOCs) represents a promising strategy of plant-beneficial bacteria to control soil-borne phytopathogens.
Pseudomonas sp. PICF6 and Pseudomonas simiae PICF7 are two indigenous inhabitants of olive roots displaying effective biological control against Verticillium dahliae. Additionally, strain PICF7 is able to promote the growth of barley and Arabidopsis thaliana, VOCs being involved in the growth of the latter species.
In this study, the antagonistic capacity of these endophytic bacteria against relevant phytopathogens (Verticillium spp., Rhizoctonia solani, Sclerotinia sclerotiorum and Fusarium oxysporum f.sp. lycopersici) was assessed. Under in vitro conditions, PICF6 and PICF7 were only able to antagonize representative isolates of V. dahliae and V. longisporum. Remarkably, both strains produced an impressive portfolio of up to twenty VOCs, that included compounds with reported antifungal (e.g., 1-undecene, (methyldisulfanyl) methane and 1-decene) or plant growth promoting (e.g., tridecane, 1-decene) activities. Moreover, their volatilomes differed strongly in the absence and presence of V. dahliae.
For example, when co incubated with the defoliating pathotype of V. dahliae, the antifungal compound 4-methyl-2,6-bis(2-methyl-2-propanyl)phenol was produced. Results suggest that volatiles emitted by these endophytes may differ in their modes of action, and that potential benefits for the host needs further investigation in planta.
Soil microbial communities are crucial for plant growth and are already depleted by anthropogenic activities.
The application of microbial transplants provides a strategy to restore beneficial soil traits, but less is known about the microbiota of traditional inoculants used in biodynamic agriculture.
In this study, we used amplicon sequencing and quantitative PCR to decipher microbial communities of composts, biodynamic manures, and plant preparations from Austria and France.
In addition, we investigated the effect of extracts derived from biodynamic manure and compost on the rhizosphere microbiome of apple trees. Microbiota abundance, composition, and diversity of biodynamic manures, plant preparations, and composts were distinct. Microbial abundances ranged between 1010-1011 (bacterial 16S rRNA genes) and 109-1011 (fungal ITS genes). The bacterial diversity was significantly higher in biodynamic manures compared to compost without discernible differences in abundance. Fungal diversity was not significantly different while abundance was increased in biodynamic manures. The microbial communities of biodynamic manures and plant preparations were specific for each production site, but all contain potentially plant-beneficial bacterial genera.
When applied in apple orchards, biodynamic preparations (extracts) had the non-significant effect of reducing bacterial and fungal abundance in apple rhizosphere (4 months post-application), while increasing fungal and lowering bacterial Shannon diversity.
One to four months after inoculation, individual taxa indicated differential abundance. We observed the reduction of the pathogenic fungus Alternaria, and the enrichment of potentially beneficial bacterial genera such as Pseudomonas.
Our study paves way for the science-based adaptation of empirically developed biodynamic formulations under different farming practices to restore the vitality of agricultural soils.
Background: Microbiome assembly was identified as an important factor for plant growth and health, but this process is largely unknown, especially for the fruit microbiome. Therefore, we analyzed strawberry plants of two cultivars by focusing on microbiome tracking during the different growth stages and storage using amplicon sequencing, qPCR, and microscopic approaches. <br /> Results: Strawberry plants carried a highly diverse microbiome, therein the bacterial families Sphingomonadaceae (25%), Pseudomonadaceae (17%), and Burkholderiaceae (11%); and the fungal family Mycosphaerella (45%) were most abundant. All compartments were colonized by high number of bacteria and fungi (10(7)-10(10) marker gene copies per g fresh weight), and were characterized by high microbial diversity (6049 and 1501 ASVs); both were higher for the belowground samples than in the phyllosphere. Compartment type was the main driver of microbial diversity, structure, and abundance (bacterial: 45%; fungal: 61%) when compared to the cultivar (1.6%; 2.2%). Microbiome assembly was strongly divided for belowground habitats and the phyllosphere; only a low proportion of the microbiome was transferred from soil via the rhizosphere to the phyllosphere. During fruit development, we observed the highest rates of microbial transfer from leaves and flowers to ripe fruits, where most of the bacteria occured inside the pulp. In postharvest fruits, microbial diversity decreased while the overall abundance increased. Developing postharvest decay caused by Botrytis cinerea decreased the diversity as well, and induced a reduction of potentially beneficial taxa. <br /> Conclusion: Our findings provide insights into microbiome assembly in strawberry plants and highlight the importance of microbe transfer during fruit development and storage with potential implications for food health and safety.
Volatile organic compounds (VOCs) are involved in microbial interspecies communication and in the mode of action of various antagonistic interactions. They are important for balancing host-microbe interactions and provide the basis for developing biological control strategies to control plant pathogens.
We studied the interactions between the bacterial antagonist Serratia plymuthica HRO-C48 and three fungal plant pathogens Rhizoctonia solani, Leptosphaeria maculans and Verticillium longisporum. Significant differences in fungal growth inhibition by the Serratia-emitted VOCs in pairwise dual culture assays and changes in the transcriptome of the bacterium and in the volatilomes of both interacting partners were observed. Even though the rate of fungal growth inhibition by Serratia was variable, the confrontation of the bacterium with the VOCs of all three fungi changed the levels of expression of the genes involved in stress response, biofilm formation, and the production of antimicrobial VOCs. Pairwise interacting microorganisms switched between defense (downregulation of gene expression) and attack (upregulation of gene expression and metabolism followed by growth inhibition of the interacting partner) modes, subject to the combinations of microorganisms that were interacting.
In the attack mode HRO-C48 significantly inhibited the growth of R. solani while simultaneously boosting its own metabolism; by contrast, its metabolism was downregulated when HRO-C48 went into a defense mode that was induced by the L. maculans and V. longisporum VOCs. L. maculans growth was slightly reduced by the one bacterial VOC methyl acetate that induced a strong downregulation of expression of genes involved in almost all metabolic functions in S. plymuthica.
Similarly, the interaction between S. plymuthica and V. longisporum resulted in an insignificant growth reduction of the fungus and repressed the rate of bacterial metabolism on the transcriptional level, accompanied by an intense volatile dialogue. Overall, our results indicate that VOCs substantially contribute to the highly break species-specific interactions between pathogens and their natural antagonists and thus deserving of increased consideration for pathogen control.
Microbiomes have an immense potential to enhance plant resilience to various biotic and abiotic stresses. However, intrinsic microbial communities respond to changes in their host's physiology and environment during plant's life cycle. The potential of the inherent plant microbiome has been neglected for a long time, especially for the postharvest period. Currently, close to 50% of all produced fruits and vegetables are lost either during production or storage. Biological control of spoilage and storage diseases is still lacking sufficiency. Today, novel multiomics technologies allow us to study the microbiome and its responses on a community level, which will help to advance current classic approaches and develop more effective and robust microbiome-based solutions for fruit and vegetable storability, quality, and safety.
The Brassica napus seed microbiota is cultivar-specific and transmitted via paternal breeding lines
(2022)
Seed microbiota influence germination and plant health and have the potential to improve crop performance, but the factors that determine their structure and functions are still not fully understood.
Here, we analysed the impact of plant-related and external factors on seed endophyte communities of 10 different oilseed rape (Brassica napus L.) cultivars from 26 field sites across Europe.
All seed lots harboured a high abundance and diversity of endophytes, which were dominated by six genera: Ralstonia, Serratia, Enterobacter, Pseudomonas, Pantoea, and Sphingomonas.
The cultivar was the main factor explaining the variations in bacterial diversity, abundance and composition. In addition, the latter was significantly influenced by diverse biotic and abiotic factors, for example host germination rates and disease resistance against Plasmodiophora brassicae.
A set of bacterial biomarkers was identified to discriminate between characteristics of the seeds, for example Sphingomonas for improved germination and Brevundimonas for disease resistance.
Application of a Bayesian community approach suggested vertical transmission of seed endophytes, where the paternal parent plays a major role and might even determine the germination performance of the offspring.
This study contributes to the understanding of seed microbiome assembly and underlines the potential of the microbiome to be implemented in crop breeding and biocontrol programmes.
Trade-off for survival
(2022)
The environmental micmbiota is increasingly exposed to chemical pollution. While the emergence of multi-resistant pathogens is recognized as a global challenge, our understanding of antimicrobial resistance (AMR) development from native microbiomes and the risks associated with chemical exposure is limited. By implementing a lichen as a bioindicator organism and model for a native microbiome, we systematically examined responses towards antimicrobials (colistin, tetracycline, glyphosate, and alkylpyrazine). Despite an unexpectedly high resilience, we identified potential evolutionary consequences of chemical exposure in terms of composition and functioning of native bacterial communities. Major shifts in bacterial composition were observed due to replacement of naturally abundant taxa; e.g. Chthoniobacterales by Pseudomonadales. A general response, which comprised activation of intrinsic resistance and parallel reduction of metabolic activity at RNA and protein levels was deciphered by a multi-omics approach. Targeted analyses of key taxa based on metagenome-assembled genomes reflected these responses but also revealed diversified strategies of their players. Chemical-specific responses were also observed, e.g., glyphosate enriched bacterial r-strategists and activated distinct ARGs. Our work demonstrates that the high resilience of the native micmbiota toward antimicrobial exposure is not only explained by the presence of antibiotic resistance genes but also adapted metabolic activity as a trade-off for survival. Moreover, our results highlight the importance of native microbiomes as important but so far neglected AMR reservoirs. We expect that this phenomenon is representative for a wide range of environmental microbiota exposed to chemicals that potentially contribute to the emergence of antibiotic-resistant bacteria from natural environments.
The desiccation of the Aral Sea represents one of the largest human-made environmental regional disasters. The salt- and toxin-enriched dried-out basin provides a natural laboratory for studying ecosystem functioning and rhizosphere assembly under extreme anthropogenic conditions.
Here, we investigated the prokaryotic rhizosphere communities of the native pioneer plant Suaeda acuminata (C.A.Mey.) Moq. in comparison to bulk soil across a gradient of desiccation (5, 10, and 40 years) by metagenome and amplicon sequencing combined with quantitative PCR (qPCR) analyses. The rhizosphere effect was evident due to significantly higher bacterial abundances but less diversity in the rhizosphere compared to bulk soil. Interestingly, in the highest salinity (5 years of desiccation), rhizosphere functions were mainly provided by archaeal communities.
Along the desiccation gradient, we observed a significant change in the rhizosphere microbiota, which was reflected by (i) a decreasing archaeon-bacterium ratio, (ii) replacement of halophilic archaea by specific plant-associated bacteria, i.e., Alphaproteobacteria and Actinobacteria, and (iii) an adaptation of specific, potentially plant-beneficial biosynthetic pathways.
In general, both bacteria and archaea were found to be involved in carbon cycling and fixation, as well as methane and nitrogen metabolism.
Analysis of metagenome-assembled genomes (MAGs) showed specific signatures for production of osmoprotectants, assimilatory nitrate reduction, and transport system induction.
Our results provide evidence that rhizosphere assembly by cofiltering specific taxa with distinct traits is a mechanism which allows plants to thrive under extreme conditions. Overall, our findings highlight a function-based rhizosphere assembly, the importance of plant-microbe interactions in salinated soils, and their exploitation potential for ecosystem restoration approaches.IMPORTANCE
The desertification of the Aral Sea basin in Uzbekistan and Kazakhstan represents one of the most serious anthropogenic environmental disasters of the last century. Since the 1960s, the world's fourth-largest inland body of water has been constantly shrinking, which has resulted in an extreme increase of salinity accompanied by accumulation of many hazardous and carcinogenic substances, as well as heavy metals, in the dried-out basin.
Here, we investigated bacterial and archaeal communities in the rhizosphere of pioneer plants by combining classic molecular methods with amplicon sequencing as well as metagenomics for functional insights.
By implementing a desiccation gradient, we observed (i) remarkable differences in the archaeon-bacterium ratio of plant rhizosphere samples, (ii) replacement of archaeal indicator taxa during succession, and (iii) the presence of specific, potentially plant-beneficial biosynthetic pathways in archaea present during the early stages.
In addition, our results provide hitherto-undescribed insights into the functional redundancy between plant-associated archaea and bacteria.
The desertification of the Aral Sea basin in Uzbekistan and Kazakhstan represents one of the most serious anthropogenic environmental disasters of the last century.
Since the 1960s, the world's fourth-largest inland body of water has been constantly shrinking, which has resulted in an extreme increase of salinity accompanied by accumulation of many hazardous and carcinogenic substances, as well as heavy metals, in the dried-out basin.
Multi-species biofilms are more resistant against stress compared to single-species biofilms. However, the mechanisms underlying this common observation remain elusive. Therefore, we studied biofilm formation of well-known opportunistic pathogens (Acinetobacter baumanii, Enterococcus faecium, Escherichia coli, Staphylococcus haemolyticus and Stenotrophomonas maltophilia) in various approaches. Synergistic effects in their multi species biofilms were observed. Using metatranscriptomics, changes in the gene expression of the involved members became evident, and provided explanations for the improved survivability under nutrient limitation and exposure to disinfectants. Genes encoding proteins for vitamin B6 synthesis and iron uptake were linked to synergism in the multi-species biofilm under nutrient-limited conditions. Our study indicates that sub-lethal concentrations of an alcohol-based disinfectant enhance biofilm yields in multi-species assemblages. A reduction of the dominant taxa in the multi-species biofilm under disinfectant pressure allowed minor taxa to bloom. The findings underline the importance of minor but antimicrobial-resistant species that serve as "protectors" for the whole assemblage due to upregulation of genes involved in defence mechanisms and biofilm formation. This ultimately results in an increase in the total yield of the multi-species biofilm. We conclude that inter-species interactions may be crucial for the survival of opportunistic pathogens; especially under conditions that are typically found under hospital settings.
Bacterial-fungal interactions under agricultural settings: from physical to chemical interactions
(2022)
Bacteria and fungi are dominant members of environmental microbiomes. Various bacterial-fungal interactions (BFIs) and their mutual regulation are important factors for ecosystem functioning and health.
Such interactions can be highly dynamic, and often require spatiotemporally resolved assessments to understand the interplay which ranges from antagonism to mutualism. Many of these interactions are still poorly understood, especially in terms of the underlying chemical and molecular interplay, which is crucial for inter-kingdom communication and interference. BFIs are highly relevant under agricultural settings; they can be determinative for crop health.
Advancing our knowledge related to mechanisms underpinning the interactions between bacteria and fungi will provide an extended basis for biological control of pests and pathogens in agriculture.
Moreover, it will facilitate a better understanding of complex microbial community networks that commonly occur in nature. This will allow us to determine factors that are crucial for community assembly under different environmental conditions and pave the way for constructing synthetic communities for various biotechnological applications. Here, we summarize the current advances in the field of BFIs with an emphasis on agriculture.