Transient microbial architects: tracing the legacy effects of ephemeral taxa during plant microbiome assembly.

BackgroundIt is known that during plant community assembly, the early colonizing species can affect the establishment, growth or reproductive success of later arriving species, often resulting in unpredictable assembly outcomes. These so called ‘priority effects’ have recently been hypothesized to work through niche-based processes, with early colonizing species either inhibiting the colonization of other species of the same niche through niche preemption, or affecting the colonization success of species of different niches through niche modification. With most work on priority effects performed in controlled, short-term mesocosm experiments, we have little insight in how niche preemption and niche modification processes interact to shape the community composition of natural vegetations. In this study, we used a functional trait approach to identify potential niche-based priority effects in restored semi-natural grasslands. More specifically, we imposed two treatments that strongly altered the community’s functional trait composition; removal of all graminoid species and removal of all legume species, and we compared progressing assembly with unaltered control plots.ResultsOur results showed that niche preemption effects can be, to a limited extent, relieved by species removal. This relief was observed for competitive grasses and herbs, but not for smaller grassland species. Although competition effects acting within functional groups (niche preemption) occurred for graminoids, there were no such effects for legumes. The removal of legumes mainly affected functionally unrelated competitive species, likely through niche modification effects of nitrogen fixation. On the other hand, and contrary to our expectations, species removal was after 4 years almost completely compensated by recolonization of the same species set, suggesting that priority effects persist after species removal, possibly through soil legacy effects.ConclusionsOur results show that both niche modification and niche preemption priority effects can act together in shaping community composition in a natural grassland system. Although small changes in species composition occurred, the removal of specific functional groups was almost completely compensated by recolonization of the same species. This suggests that once certain species get established, it might prove difficult to neutralize their effect on assembly outcome, since their imposed priority effects might act long after their removal.Electronic supplementary materialThe online version of this article (doi:10.1186/s12898-016-0077-9) contains supplementary material, which is available to authorized users.

Synthetic Communities (SynComs) are being developed and tested to manipulate plant microbiota and improve plant health. To date, only few studies proposed the use of SynCom on seed despite its potential for plant microbiota engineering. We developed and presented a simple and effective seedling microbiota engineering method using SynCom inoculation on seeds. The method was successful using a wide diversity of SynCom compositions and bacterial strains that are representative of the common bean seed microbiota. First, this method enables the modulation of seed microbiota composition and community size. Then, SynComs strongly outcompeted native seed and potting soil microbiota and contributed on average to 80% of the seedling microbiota. We showed that strain abundance on seed was a main driver of an effective seedling microbiota colonization. Also, selection was partly involved in seed and seedling colonization capacities since strains affiliated to Enterobacteriaceae and Erwiniaceae were good colonizers while Bacillaceae and Microbacteriaceae were poor colonizers. Additionally, the engineered seed microbiota modified the recruitment and assembly of seedling and rhizosphere microbiota through priority effects. This study shows that SynCom inoculation on seeds represents a promising approach to study plant microbiota assembly and its consequence on plant fitness.

Plant microbiota dysbiosis and the Anna Karenina Principle.

Priority effects, the effects of early-arriving species on late-arriving species, are caused by niche preemption and/or niche modification. The strength of priority effects can be determined by the extent of niche preemption and/or modification by the early-arriving species; however, the strength of priority effects may also be influenced by the late-arriving species, as some species may be better adapted to deal with niche preemption and/or modification. Therefore, some combinations of species will likely lead to stronger priority effects than others. We tested priority effects for all pairwise combinations of 15 plant species, including grasses, legumes, and nonleguminous forbs, by comparing simultaneous and sequential arrival orders in a 10-week-long, controlled, pot experiment. We did this by using the competitive effect and response framework, quantifying the ability to suppress a neighbor as the competitive effect and the ability to tolerate a neighbor as the competitive response. We found that when arriving simultaneously, species that caused strong competitive effects also had weaker competitive responses. When arriving sequentially, species that caused strong priority effects when arriving early also had weaker responses to priority effects when arriving late. Among plant functional groups, legumes had the weakest response to priority effects. We also measured plant functional traits related to the plant economic spectrum, which were combined into a principal components analysis (PCA) where the first axis represented a conservative-to-acquisitive trait gradient. Using the PCA species scores, we showed that both the traits of the focal and the neighboring species determined the outcome of competition. Trait dissimilarities between the focal and neighboring species were more important when species arrived sequentially than when species arrived simultaneously. Specifically, priority effects only became weaker when the late-arriving species was more acquisitive than the early-arriving species. Together, our findings show that traits and specifically the interaction of traits between species are more important in determining competition outcomes when species arrive sequentially (i.e., with priority effects present) than when arriving simultaneously.

Mitogen-activated protein kinase (MAPK) cascades are highly conserved signaling modules that coordinate diverse biological processes such as plant innate immunity and development. Recently, MAPK cascades have emerged as pivotal regulators of the plant holobiont, influencing the assembly of normal plant microbiota, essential for maintaining optimal plant growth and health. In this review, we provide an overview of current knowledge on MAPK cascades, from upstream perception of microbial stimuli to downstream host responses. Synthesizing recent findings, we explore the intricate connections between MAPK signaling and the assembly and functioning of plant microbiota. Additionally, the role of MAPK activation in orchestrating dynamic changes in root exudation to shape microbiota composition is discussed. Finally, our review concludes by emphasizing the necessity for more sophisticated techniques to accurately decipher the role of MAPK signaling in establishing the plant holobiont relationship.

How does plant sex alter microbiota assembly in dioecious plants?

The order and timing of species immigration during community assembly can affect species abundances at multiple spatial scales. Known as priority effects, these effects cause historical contingency in the structure and function of communities, resulting in alternative stable states, alternative transient states, or compositional cycles. The mechanisms of priority effects fall into two categories, niche preemption and niche modification, and the conditions for historical contingency by priority effects can be organized into two groups, those regarding regional species pool properties and those regarding local population dynamics. Specifically, two requirements must be satisfied for historical contingency to occur: The regional pool contains species that can together cause priority effects, and local dynamics are rapid enough for early-arriving species to preempt or modify niches before other species arrive. Organizing current knowledge this way reveals an outstanding key question: How are regional species pools that yield priority effects generated and maintained?

Plants are in intimate association with taxonomically structured microbial communities called the plant microbiota. There is growing evidence that the plant microbiota contributes to the holistic performance and general health of plants, especially under unfavorable situations. Despite the attached benefits, surprisingly, the plant microbiota in nature also includes potentially pathogenic strains, signifying that the plant hosts have tight control over these microbes. Despite the conceivable role of plant immunity in regulating its microbiota, we lack a complete understanding of its role in governing the assembly, maintenance, and function of the plant microbiota. Here, we highlight the recent progress on the mechanistic relevance of host immunity in orchestrating plant-microbiota dialogues and discuss the pluses and perils of these microbial assemblies.

Abiotic stress adversely affects cellular homeostasis and ultimately impairs plant growth, posing a serious threat to agriculture. Climate change modeling predicts increasing occurrences of abiotic stresses such as drought and extreme temperature, resulting in decreasing the yields of major crops such as rice, wheat, and maize, which endangers food security for human populations. Plants are associated with diverse and taxonomically structured microbial communities that are called the plant microbiota. Plant microbiota often assist plant growth and abiotic stress tolerance by providing water and nutrients to plants and modulating plant metabolism and physiology and, thus, offer the potential to increase crop production under abiotic stress. In this review, we summarize recent progress on how abiotic stress affects plants, microbiota, plant-microbe interactions, and microbe-microbe interactions, and how microbes affect plant metabolism and physiology under abiotic stress conditions, with a focus on drought, salt, and temperature stress. We also discuss important steps to utilize plant microbiota in agriculture under abiotic stress.[Formula: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Biotic and abiotic stresses are the main problems affecting agricultural losses. Consequently, understanding the mechanisms underlying plant resistance or tolerance helps us to develop fruitful new agricultural strategies. These will allow us to face the challenges of producing food for a growing human population in a sustainable and environmentally friendly way. To compensate for their sessile life and face a broad range of biotic and abiotic stresses, plants have evolved a wide range of survival and adaptation strategies. Amongst them, higher plants are capable of inducing some stress “memory,” or “stress imprinting.” Bruce et al. (2007) define stress imprinting as genetic or biochemical modifications induced by a first stress exposure that leads to enhanced resistance to a later stress. This phenomenon also known as “priming” results in a faster and stronger induction of basal resistance mechanisms upon subsequent pathogen attack, or greater tolerance against abiotic stresses (Pastor et al., 2013). Basal resistance by itself is too weak to protect against virulent pathogens, since it constitutes a residual level of resistance after immune suppression by the pathogen through co-evolution (Walters and Heil, 2007; Conrath, 2011). However, Ahmad et al. (2010) proposed that priming-inducing stimuli can provide more effective basal resistance, particularly when an earlier defense response precedes immune suppression by the invading pathogen. Following perception of microbe-associated molecular patterns (MAMPs), recognition of pathogen-derived effectors or colonization by beneficial microbes, priming can also be induced by treatment with some natural or synthetic compounds or even by wounding (Conrath, 2011). Through priming plants are able to induce responses to a range of biotic and abiotic stresses, providing low-cost protection in relatively high stress-pressure conditions. Despite priming phenomena having been widely described, the molecular mechanisms of defense priming are still unclear. Such techniques are now starting to emerge as a promising alternative for sustainable modern pest management in the field, since some pesticides have been shown to actually exert their known plant health- and yield-increasing effects through priming (Beckers and Conrath, 2007). From an ecological point of view, the benefits of priming are clear: rather than leading to the costly and potentially wasteful activation of defenses, a metabolic state of alert is induced after an initial infection, enabling a rapid intense resistance response to subsequent attacks. Thus, this strategy appears promising for crop protection purposes (Walters and Heil, 2007).

Our skin and mucosal surfaces are colonized by diverse microbial communities, collectively known as the microbiota [1]. The microbiota provides benefits as microbial metabolites contribute to host nutrition and immune education, although the viability of germ-free animals conjectures that these two functions are not essential for life. However, environmental exposure makes germ-free animals prone to lethal infection, illustrating that the microbiota confers a third function that is often vital, namely, the ability to confer colonization resistance against pathogens [2]. Colonization resistance is an acquired trait, because the microbiota is assembled after birth by attaining maternal and environmental microbes [3]. To coexist, each species within the microbial community needs to be able to utilize a critical resource better than any other member of the microbiota, and the abundance of this growth-limiting resource determines the abundance of the species, a concept known as the nutrient-niche hypothesis [4]. The conceptual framework of the nutrient-niche hypothesis suggests that the neonate microbiota will mature until all discrete nutrient-niches have been filled with a suitable occupant, thereby reaching an equilibrium state [5]. Assuming the same anatomical location in different individuals exposes similar nutrient-niches, the nutrient-niche hypothesis further predicts that the metabolic pathways that enable each member within the microbial community to utilize its growth-limiting nutrient must be conserved between different individuals. Consistent with this prediction, metabolic pathways encoded by the microbiota are very similar between individuals [1]. However, carriage of microbial taxa varies greatly within a healthy population [1], an observation that is not explained by the nutrient-niche hypothesis and remains poorly understood. Priority effects generate variation in taxa carriage Host genetic variation explains only a small fraction of taxonomic microbiota variation between individuals, whereas environmental influences dominate this trait [6]. An important environmental influence in the gastrointestinal tract is the diet, which determines the availability of a subset of growth-limiting nutrients, thereby adding or subtracting nutrient-niches [7, 8]. For example, microbiota-accessible carbohydrates found in dietary fiber determine the abundance of fiber-consuming saccharolytic bacteria in the gut microbiota, and prolonged dietary fiber starvation can lead to an irreversible extinction of species specialized in devouring this critical resource by eliminating their nutrient-niche [8]. Although diet can generate statistically significant changes in the taxonomic composition of the gut microbiota, these changes are small compared to the variation observed between individuals. Furthermore, diet does not provide a plausible explanation for the taxonomic diversity observed in microbial communities outside the gastrointestinal tract [1]. Instead, a critical factor generating taxonomic microbiota diversity between individuals is the order of species arrival and timing by which host surfaces are colonized early in life [9]. The colonization order influences both the outcome of microbial community assembly and the ecological success of individual microbes [3, 9]. These priority effects are preserved in mice lacking adaptive immunity, suggesting that acquired host responses are not a major source of taxonomic diversity in the microbiota composition [9]. Priority effects are mediated through niche preemption or niche modification and can involve the genetic adaptation of microbes to a niche [9, 12], but the underlying mechanisms are incompletely understood. Mechanistic insights into this “first come, first serve” phenomenon suggest that the microbe that initially occupies a nutrient-niche in a neonate gains priority access to the growth-limiting nutrient that defines its nutrient-niche [10]. A growth-limiting resource that determines the abundance of facultative anaerobic Enterobacteriaceae (phylum Proteobacteria) within the microbiota of the large intestine is the availability of respiratory electron acceptors, such as oxygen [11]. Escherichia coli (family Enterobacteriaceae) has access to oxygen in the ceca of neonate chicks when it is inoculated one day prior to challenge with Salmonella enterica (family Enterobacteriaceae) but not when neonate chicks receive both species at the same time [10], suggesting that order and timing of gut colonization determine whether growth-limiting resources are accessible to a microbe. Henceforth we will refer to the concept that the founding occupant gains priority access to the growth-limiting resource that defines its nutrient-niche as the “founder hypothesis.” The founder hypothesis suggests that stochastic effects that govern the initial exposure of neonates to microbes that become founding occupants of each nutrient-niche are a prominent source of taxonomic variation in the microbiota composition between individuals (Fig 1) [3]. Open in a separate window Fig 1 The founder hypothesis. The principles of the founder hypothesis are shown schematically for a single nutrient-niche. Stochastic effects governing microbial exposure during infancy determine which microbial species (red or blue rods) establishes residency in the nutrient-niche, thereby generating diversity in taxa carriage between individuals. The founding occupant gains priority access to the growth-limiting resource that defines its nutrient-niche. These priority effects enable the occupant to confer colonization resistance against environmental exposure to microorganisms that are suitable contenders for the same nutrient-niche. The resulting resistance to stress imposed through environmental exposure to microorganisms produces microbiota resistance.

SummaryThe interaction of plants with complex microbial communities is the result of co‐evolution over millions of years and contributed to plant transition and adaptation to land. The ability of plants to be an essential part of complex and highly dynamic ecosystems is dependent on their interaction with diverse microbial communities. Plant microbiota can support, and even enable, the diverse functions of plants and are crucial in sustaining plant fitness under often rapidly changing environments. The composition and diversity of microbiota differs between plant and soil compartments. It indicates that microbial communities in these compartments are not static but are adjusted by the environment as well as inter‐microbial and plant–microbe communication. Hormones take a crucial role in contributing to the assembly of plant microbiomes, and plants and microbes often employ the same hormones with completely different intentions. Here, the function of hormones as go‐betweens between plants and microbes to influence the shape of plant microbial communities is discussed. The versatility of plant and microbe‐derived hormones essentially contributes to the creation of habitats that are the origin of diversity and, thus, multifunctionality of plants, their microbiota and ultimately ecosystems.

Flowers serve as hubs for biotic interactions with pollinators and microbes, which can significantly impact plant reproduction and health. Previous studies have shown that the flower microbiota undergoes dynamic assembly processes during anthesis. However, the influence of foraging pollinators on the assembly and dispersal of the flower microbiota and the transmission of plant pathogens remains poorly understood. In this study, we used insect exclusion netting to investigate the role of pollinators in the assembly of the microbiota on apple stigma and the transmission of the fire blight pathogen Erwinia amylovora. We found that excluding pollinators had a minor impact on the community diversity and composition of the apple stigma microbiota, while the flower's developmental stage had a strong influence. Additionally, pollinator exclusion altered bacterial dispersal and the relative abundance of different bacterial species, including E. amylovora, suggesting that pollinators play a role in transmitting plant pathogens. Using a reporter system, we demonstrated that bumble bees can transmit the fire blight pathogen from an infected flower under controlled growth conditions. Our study highlights the importance of intrinsic and pollinator-independent microbes as sources of inoculum for the stigma microbiota and underscores the role of foraging pollinators in vectoring plant pathogens.

Deserts are predicted to be one of the ecosystems most vulnerable to global climate change, with dramatic fluctuations of temperature and water, even over the span of a single day. These previous disturbances could influence the response of the soil microbiome and its functions to subsequent disturbances, which is known as legacy effect. However, how legacy effects shape the response of soil microbiome and its functions to environmental fluctuations (e.g. temperature and water availability) in desert ecosystems remains to be investigated. Here, we firstly exposed desert soils to drought, freezing or their combination, and then followed by a second disturbance, resulting in a temporally full factorial treatment. We found that environmental change legacies affected the response of soil multifunctionality, microbial abundance and richness to second drought and freezing, except for eukaryotic richness. Initial disturbances caused legacy effects on microbial composition and weakened their responses to later disturbances, and these effects were stronger for prokaryotes than eukaryotes. The attenuated response to later disturbances is largely due to that almost half of the taxa affected by the earlier disturbances were also affected by the second disturbances. The phylogenetic depth of these responses varied minimally among the types of disturbances but were more conserved for negative responses, indicating a result of historical adaptation. Moreover, the altered community composition was associated with functional changes in the disturbed soils. These findings will improve our understanding of the mechanisms underlying the legacy impacts of multiple environmental disturbances on desert microbial communities and strengthen our ability to develop management strategies for protection prior to disturbance events. Read the free Plain Language Summary for this article on the Journal blog.

Human microbiota assembly commences at birth, seeded by both maternal and environmental microorganisms. Ecological theory postulates that primary colonizers dictate microbial community assembly outcomes, yet such microbial priority effects in the human gut remain underexplored. Here using longitudinal faecal metagenomics, we characterized neonatal microbiota assembly for a cohort of 1,288 neonates from the UK. We show that the pioneering neonatal gut microbiota can be stratified into one of three distinct community states, each dominated by a single microbial species and influenced by clinical and host factors, such as maternal age, ethnicity and parity. A community state dominated by Enterococcus faecalis displayed stochastic microbiota assembly with persistent high pathogen loads into infancy. In contrast, community states dominated by Bifidobacterium, specifically B. longum and particularly B. breve, exhibited a stable assembly trajectory and long-term pathogen colonization resistance, probably due to strain-specific functional adaptions to a breast milk-rich neonatal diet. Consistent with our human cohort observation, B. breve demonstrated priority effects and conferred pathogen colonization resistance in a germ-free mouse model. Our findings solidify the crucial role of Bifidobacteria as primary colonizers in shaping the microbiota assembly and functions in early life.