The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems

Microbes are the unseen majority in soil and comprise a large portion of life's genetic diversity. Despite their abundance, the impact of soil microbes on ecosystem processes is still poorly understood. Here we explore the various roles that soil microbes play in terrestrial ecosystems with special emphasis on their contribution to plant productivity and diversity. Soil microbes are important regulators of plant productivity, especially in nutrient poor ecosystems where plant symbionts are responsible for the acquisition of limiting nutrients. Mycorrhizal fungi and nitrogen-fixing bacteria are responsible for c. 5–20% (grassland and savannah) to 80% (temperate and boreal forests) of all nitrogen, and up to 75% of phosphorus, that is acquired by plants annually. Free-living microbes also strongly regulate plant productivity, through the mineralization of, and competition for, nutrients that sustain plant productivity. Soil microbes, including microbial pathogens, are also important regulators of plant community dynamics and plant diversity, determining plant abundance and, in some cases, facilitating invasion by exotic plants. Conservative estimates suggest that c. 20 000 plant species are completely dependent on microbial symbionts for growth and survival pointing to the importance of soil microbes as regulators of plant species richness on Earth. Overall, this review shows that soil microbes must be considered as important drivers of plant diversity and productivity in terrestrial ecosystems.     

Common themes in nutrient acquisition by plant symbiotic microbes,described by the Gene Ontology

A critical function for symbionts is the acquisition of nutrients from their host. Relationships between hosts and symbionts range from biotrophic mutualism to necrotrophic parasitism, with a corresponding range of structures to facilitate nutrient flow between host and symbiont. Here, we review common themes among the nutrient acquisition strategies of a range of plant symbiotic microorganisms, including mutualistic symbionts, biotrophic pathogens that feed from living tissue, necrotrophic pathogens that kill host tissue, and hemibiotrophic pathogens that switch from biotrophy to necrotrophy. We show how Gene Ontology (GO) terms developed by the Plant-Associated Microbe Gene Ontology (PAMGO) Consortium can be used for describing commonalities in nutrient acquisition among diverse plant symbionts. Where appropriate, parallels found among animal symbionts are also highlighted.     

The rhizosphere microbiome and plant health

The diversity of microbes associated with plant roots is enormous, in the order of tens of thousands of species. This complex plant-associated microbial community, also referred to as the second genome of the plant, is crucial for plant health. Recent advances in plant-microbe interactions research revealed that plants are able to shape their rhizosphere microbiome, as evidenced by the fact that different plant species host specific microbial communities when grown on the same soil. In this review, we discuss evidence that upon pathogen or insect attack, plants are able to recruit protective microorganisms, and enhance microbial activity to suppress pathogens in the rhizosphere. A comprehensive understanding of the mechanisms that govern selection and activity of microbial communities by plant roots will provide new opportunities to increase crop production.     

Functional roles of microbial symbionts in plant cold tolerance

In this review, we examine the functional roles of microbial symbionts in plant tolerance to cold and freezing stresses. The impacts of symbionts on antioxidant activity, hormonal signaling and host osmotic balance are described, including the effects of the bacterial endosymbionts Burkholderia, Pseudomonas and Azospirillum on photosynthesis and the accumulation of carbohydrates such as trehalose and raffinose that improve cell osmotic regulation and plasma membrane integrity. The influence of root fungal endophytes and arbuscular mycorrhizal fungi on plant physiology at low temperatures, for example their effects on nutrient acquisition and the accumulation of indole‐3‐acetic acid and antioxidants in tissues, are also reviewed. Meta‐analyses are presented showing that aspects of plant performance (shoot biomass, relative water content, sugar and proline concentrations and F_v/F_m) are enhanced in symbiotic plants at low (?1 to 15 °C), but not at high (20–26 °C), temperatures. We discuss the implications of microbial symbionts for plant performance at low and sub‐zero temperatures in the natural environment and propose future directions for research into the effects of symbionts on the cold and freezing tolerances of plants, concluding that further studies should routinely incorporate symbiotic microbes in their experimental designs.     

Epitopic hexapeptide sequences from Baltic cod parvalbumin beta (allergen Gad c 1) are common in the universal proteome

The aim of this study was to analyze the distribution of hexapeptide fragments considered as epitopes of Baltic cod parvalbumin beta (allergen Gad c 1) in the universal proteome. Cod (Gadus morhua subsp. callarias) parvalbumin hexapeptides cataloged in the Immune Epitope Database were used as query sequences. The UniProt database was screened using the WU-BLAST 2 program. The distribution of hexapeptide fragments was investigated in various protein families, classified according to the presence of the appropriate domains, and in proteins of plant, animal and microbial species. Hexapeptides from cod parvalbumin were found in the proteins of plants and animals which are food sources, microorganisms with various applications in food technology and biotechnology, microorganisms which are human symbionts and commensals as well as human pathogens. In the last case possible coverage between epitopes from pathogens and allergens should be avoided during vaccine design.     

Effects of polymicrobial communities on host immunity and response

Microorganisms grow as members of microbial communities in unique niches, such as the mucosal surfaces of the human body. These microbial communities, containing both commensals and opportunistic pathogens, serve to keep individual pathogens 'in check' through a variety of mechanisms and complex interactions, both between the microorganisms themselves and the microorganisms and the host. Recent studies shed new light on the diversity of microorganisms that form the human microbial communities and the interactions these microbial communities have with the host to stimulate immune responses. This occurs through their recognition by dendritic cells or their ability to induce differential cytokine and defensin profiles. The differential induction of defensins by commensals and pathogens and the ability of the induced defensins to interact with the antigens from these microorganisms may attenuate proinflammatory signaling and trigger adaptive immune responses to microbial antigens in a multistep process. Such an activity may be a mechanism that the host uses to sense what is on its mucosal surfaces, as well as to differentiate among commensals and pathogens.     

A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity,plant nutrition and seedling recruitment

Highly diverse microbial assemblages colonize plant roots. It is still poorly understood whether different members of this root microbiome act synergistically by supplying different services (for example, different limiting nutrients) to plants and plant communities. In order to test this, we manipulated the presence of two widespread plant root symbionts, arbuscular mycorrhizal fungi and nitrogen-fixing rhizobia bacteria in model grassland communities established in axenic microcosms. Here, we demonstrate that both symbionts complement each other resulting in increased plant diversity, enhanced seedling recruitment and improved nutrient acquisition compared with a single symbiont situation. Legume seedlings obtained up to 15-fold higher productivity if they formed an association with both symbionts, opposed to productivity they reached with only one symbiont. Our results reveal the importance of functional diversity of symbionts and demonstrate that different members of the root microbiome can complement each other in acquiring different limiting nutrients and in driving important ecosystem functions.     

AM真菌在植物病虫害生物防治中的作用机制

丛枝菌根(Arbuscular Mycorrhizae,AM)真菌是一类广泛分布于土壤生态系统中的有益微生物,能与大约80%的陆生高等植物形成共生体。由土传病原物侵染引起的土传病害被植物病理学界认定为最难防治的病害之一。研究表明,AM真菌能够拮抗由真菌、线虫、细菌等病原体引起的土传性植物病害,诱导宿主植物增强对病虫害的耐/抗病性。当前,利用AM真菌开展病虫害的生物防治已经引起生态学家和植物病理学家的广泛关注。基于此,围绕AM真菌在植物病虫害生物防治中的最新研究进展,从AM真菌改变植物根系形态结构、调节次生代谢产物的合成、改善植物根际微环境、与病原微生物直接竞争入侵位点和营养分配、诱导植株体内抗病防御体系的形成等角度,探究AM真菌在植物病虫害防治中的作用机理,以期为利用AM真菌开展植物病虫害的生物防治提供理论依据,并对本领域未来的发展方向和应用前景进行展望。     

The diversity of soil microbial communities matters when legumes face drought

The cultivation of legumes shows promise for the development of sustainable agriculture, but yield instability remains one of the main obstacles for its adoption. Here, we tested whether the yield stability (i.e., resistance and resilience) of pea plants subjected to drought could be enhanced by soil microbial diversity. We used a dilution approach to manipulate the microbial diversity, with a genotype approach to distinguish the effect of symbionts from that of microbial diversity as a whole. We investigated the physiology of plants in response to drought when grown on a soil containing high or low level of microbial diversity. Plants grown under high microbial diversity displayed higher productivity and greater resilience after drought. Yield losses were mitigated by 15% on average in the presence of high soil microbial diversity at sowing. Our study provides proof of concept that the soil microbial community as a whole plays a key role for yield stability after drought even in plant species living in relationships with microbial symbionts. These results emphasize the need to restore soil biodiversity for sustainable crop management and climate change adaptation.     

Root exudate cocktails: the link between plant diversity and soil microorganisms?

Higher plant diversity is often associated with higher soil microbial biomass and diversity, which is assumed to be partly due to elevated root exudate diversity. However, there is little experimental evidence that diversity of root exudates shapes soil microbial communities. We tested whether higher root exudate diversity enhances soil microbial biomass and diversity in a plant diversity gradient, thereby negating significant plant diversity effects on soil microbial properties. We set up plant monocultures and two‐ and three‐species mixtures in microcosms using functionally dissimilar plants and soil of a grassland biodiversity experiment in Germany. Artificial exudate cocktails were added by combining the most common sugars, organic acids, and amino acids found in root exudates. We applied four different exudate cocktails: two exudate diversity levels (low‐ and high‐diversity) and two nutrient‐enriched levels (carbon‐ and nitrogen‐enriched), and a control with water only. Soil microorganisms were more carbon‐ than nitrogen‐limited. Cultivation‐independent fingerprinting analysis revealed significantly different soil microbial communities among exudate diversity treatments. Most notably and according to our hypothesis, adding diverse exudate cocktails negated the significant plant diversity effect on soil microbial properties. Our findings provide the first experimental evidence that root exudate diversity is a crucial link between plant diversity and soil microorganisms.     

High Diversity Revealed in Leaf‐Associated Protists (Rhizaria: Cercozoa) of Brassicaceae

The largest biological surface on earth is formed by plant leaves. These leaf surfaces are colonized by a specialized suite of leaf‐inhabiting microorganisms, recently termed “phyllosphere microbiome”. Microbial prey, however, attract microbial predators. Protists in particular have been shown to structure bacterial communities on plant surfaces, but virtually nothing is known about the community composition of protists on leaves. Using newly designed specific primers targeting the 18S rDNA gene of Cercozoa, we investigated the species richness of this common protist group on leaves of four Brassicaceae species from two different locations in a cloning‐based approach. The generated sequences revealed a broad diversity of leaf‐associated Cercozoa, mostly bacterial feeders, but also including known plant pathogens and a taxon of potential endophytes that were recently described as algal predators in freshwater systems. This initial study shows that protists must be regarded as an integral part of the microbial diversity in the phyllosphere of plants.     

细菌铁载体拮抗植物病原真菌及促生作用研究进展

铁载体是微生物在缺铁条件下分泌的小分子有机化合物,以获取铁元素维持其生长。细菌分泌的铁载体在拮抗植物病原菌和促进植物生长方面具有重要作用。本文总结了细菌铁载体拮抗植物病原真菌的营养和生态位竞争、诱导植物诱导性系统抗性、扰乱病原菌铁稳态的机制,以及促进植物生长的作用,以解释细菌分泌的铁载体在多功能微生物菌剂研制中的重要作用。     

按蚊肠道微生物及其在阻断疟疾传播上的应用

按蚊体内,尤其是中肠内定殖着大量的微生物群落。肠道菌群通过与按蚊的长期协同进化形成了相互依存的共生关系。肠道共生菌参与调节按蚊的多种生命活动,对于维持按蚊的健康发挥着重要作用,已经成为一个与宿主按蚊密不可分的重要"器官"。研究表明,肠道共生菌在按蚊物质代谢、营养、发育、生殖、免疫调控和免疫防御等生理过程中发挥着重要的调节作用。蚊虫是疟疾、登革、寨卡等多种疾病的传播媒介,而肠道共生菌对寄生虫和病毒在蚊虫肠道内的发育和感染具有重要影响,因此研究蚊虫与共生菌的相互作用有着重要的理论和实践意义。本文将对按蚊肠道共生菌的多样性、生物学功能、与宿主相互作用的机制及其在防治疟疾上的应用进展进行综述,并对未来的研究提出展望。     

Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants

Microbial communities in plant roots provide critical links between above‐ and belowground processes in terrestrial ecosystems. Variation in root communities has been attributed to plant host effects and microbial host preferences, as well as to factors pertaining to soil conditions, microbial biogeography and the presence of viable microbial propagules. To address hypotheses regarding the influence of plant host and soil biogeography on root fungal and bacterial communities, we designed a trap‐plant bioassay experiment. Replicate Populus, Quercus and Pinus plants were grown in three soils originating from alternate field sites. Fungal and bacterial community profiles in the root of each replicate were assessed through multiplex 454 amplicon sequencing of four loci (i.e., 16S, SSU, ITS, LSU rDNA). Soil origin had a larger effect on fungal community composition than did host species, but the opposite was true for bacterial communities. Populus hosted the highest diversity of rhizospheric fungi and bacteria. Root communities on Quercus and Pinus were more similar to each other than to Populus. Overall, fungal root symbionts appear to be more constrained by dispersal and biogeography than by host availability.     

Epichloë endophyte effects on leaf blotch pathogen (Rhynchosporium sp.) of tall fescue (Schedonorus phoenix) vary among grass origin and environmental conditions

ABSTRACT

Background

Systemic Epichloë endophytes are common fungal symbionts of many cool-season grasses. They are known for their capability of increasing host plant tolerance against biotic and abiotic stressors, including grass pathogens. However, results on endophyte-mediated disease resistance have been ambiguous, and the underlying mechanisms of disease resistance remain unknown.     

Pathogen incidence and their potential as microbial control agents in IPM of maize stem borers in West Africa

A review of the existing basis for maize stem borer IPM is given and the role of pathogens in the system is evaluated. Survey work outlining the major groups of insect pathogens is described; fungi (Beauveria bassiana and Metarhizium anisopliae), bacteria (Bacillus thuringiensis and Serratia marcesens), and viruses (granuloviruses and cytoplasmic polyhedroviruses) were identified. The presence of other unidentified protozoans, nematodes, fungi and viruses was noted. The virulence of some of the more promising known insect pathogens was explored in preliminary bioassays. Considering the cryptic habits of the insects, and the low input agriculture practiced by the majority of maize farmers in sub-Saharan Africa, Beauveria bassiana isolates possessing the capacity to grow systemically in the maize plant are considered one of the more interesting candidates for development as microbial control agents despite limited control in preliminary trials. Further work should also investigate the potential of pathogens of moderate virulence, such as the protozoans and CPVs.     

Effects of biodiversity in agricultural landscapes on the protective microbiome of insects – a review

Symbiotic bacteria in herbivorous insects can have strong beneficial impacts on their host's survival, including conferring resistance to natural enemies such as parasitoid wasps or pathogens, while also imposing energetic costs on the host, resulting in cost‐benefit trade‐offs. Whether these trade‐offs favour the hosting of symbionts depends on the growth environment of the herbivore. Long‐term experimental grassland studies have shown that increasing plant species richness leads to an increased diversity of associated herbivores and their natural enemies. Such a change in natural enemy diversity, related to changes in plant diversity, could also drive changes in the community of symbionts hosted by the herbivorous insects. Aphids are one model system for studying symbionts in insects, and effects of host‐plant species and diversity on aphid‐symbiont interactions have been documented. Yet, we still understand little of the mechanisms underlying such effects. We review the current state of knowledge of how biodiversity can impact aphid‐symbiont communities and the underlying drivers. Then, we discuss this in the framework of sustainable agriculture, where increased plant biodiversity, in the form of wildflower strips, is used to recruit natural enemies to crop fields for their pest control services. Although aphid symbionts have the potential to reduce biological control effectiveness through conferring protection for the host insect, we discuss how increasing plant and natural enemy biodiversity can mitigate these effects and identify future research opportunities. Understanding how to promote beneficial interactions in ecological systems can help in the development of more sustainable agricultural management strategies.     

The microbial flora of Aphis gossypii: Patterns across host plants and geographical space

The cotton aphid, Aphis gossypii, has a worldwide distribution and causes damage to numerous economically important crops. The bacterial symbionts associated with cotton aphids, sampled mainly from malvaceous and cucurbitaceous plants within Japan and Australia, were characterised using molecular profiling approaches. The goal was to document the aphid symbionts present and determine if patterns of microbial diversity are consistent with the existence of host plant related cryptic species in A. gossypii. The bacterial profiles of the aphids are diverse and reflect local geography more than host plant use.     

Defensive properties of pyrrolizidine alkaloids against microorganisms

The understanding of the selection factors that drive chemical diversification of secondary metabolites of constitutive defence systems in plants, such as pyrrolizidine alkaloids (PAs), is still incomplete. Historically, plants always have been confronted with microorganisms. Long before herbivores existed on this planet, plants had to cope with microbial pathogens. Therefore, plant pathogenic microorganisms may have played an important role in the early evolution of the secondary metabolite diversity. In this review, we discuss the impact that plant-produced PAs have on plant-associated microorganisms. The objective of the review is to present the current knowledge on PAs with respect to anti-microbial activities, adaptation and detoxification by microorganisms, pathogenic fungi, root protection and PA induction. Many in vitro experiments showed effects of PAs on microorganisms. These results point to the potential of microorganisms to be important for the evolution of PAs. However, only a few in vivo studies have been published and support the results of the in vitro studies. In conclusion, the topics pointed out in this review need further exploration by carrying out ecological experiments and field studies.     

Genome evolution in filamentous plant pathogens: why bigger can be better

Many species of fungi and oomycetes are plant pathogens of great economic importance. Over the past 7 years, the genomes of more than 30 of these filamentous plant pathogens have been sequenced, revealing remarkable diversity in genome size and architecture. Whereas the genomes of many parasites and bacterial symbionts have been reduced over time, the genomes of several lineages of filamentous plant pathogens have been shaped by repeat-driven expansions. In these lineages, the genes encoding proteins involved in host interactions are frequently polymorphic and reside within repeat-rich regions of the genome. Here, we review the properties of these adaptable genome regions and the mechanisms underlying their plasticity, and we illustrate cases in which genome plasticity has contributed to the emergence of new virulence traits. We also discuss how genome expansions may have had an impact on the co-evolutionary conflict between these filamentous plant pathogens and their hosts.