The Plant-Associated Microbe Gene Ontology (PAMGO) Consortium: community development of new Gene Ontology terms describing biological processes involved in microbe-host interactions

All microbes that form beneficial, neutral, or pathogenic associations with hosts face similar challenges. They must physically adhere to and/or gain entry to host tissues; they must avoid, suppress, or tolerate host defenses; they must acquire nutrients from the host and successfully multiply. Microbes that associate with hosts come from many kingdoms of life and include bacteria, fungi, oomycetes, and nematodes. The increasing numbers of full genome sequences from these diverse microbes provide the opportunity to discover common mechanisms by which the microbes forge and maintain intimate associations with host organisms. However, cross-genome analyses have been hindered by lack of a universal vocabulary for describing biological processes involved in the interplay between microbes and their hosts. The Plant-Associated Microbe Gene Ontology (PAMGO) Consortium has been working for three years as an official interest group of the Gene Ontology (GO) Consortium to develop well-defined GO terms that describe many of the biological processes common to diverse plant- and animal-associated microbes. Creating these terms, over 700 at this time, has required a synthesis of diverse points of view from many research communities. The use of these terms in genome annotation will allow cross-genome searches for genes with common function (without demand for sequence similarity) and also improve the interpretation of data from high-throughput microarray and proteomic analyses. This article, and the more focused mini-reviews that make up this supplement to BMC Microbiology, describe the development and use of these terms.     

The intracellular pathogen concept

The intracellular pathogen concept classifies pathogenic microbes on the basis of their site of replication and dependence on host cells. This concept played a fundamental role in establishing the field of cellular microbiology, founded in part by Dr. Pascale Cossart, whose seminal contributions are honored in this issue of Molecular Microbiology. The recognition that microbes can access and replicate in privileged compartments within host cells has led to many new and fruitful lines of investigation into the biology of the cell and mechanisms of cell-mediated immunity. However, like any scientific concept, the intracellular pathogen concept can become a dogma that constrains thinking and oversimplifies complex and dynamic host–pathogen interactions. Growing evidence has blurred the distinction between “intracellular” and “extracellular” pathogens and demonstrated that many pathogens can exist both within and outside of cells. Although the intracellular pathogen concept remains useful, it should not be viewed as a rigid classification of pathogenic microbes, which exhibit remarkable variation and complexity in their behavior in the host.     

The ecological potentials of Phytomyxea (“plasmodiophorids”) in aquatic food webs

The Phytomyxea (“plasmodiophorids”) including both Plasmodiophorida and Phagomyxida is a monophyletic group of Eukaryotes composed of obligate biotrophic parasites of green plants, brown algae, diatoms and stramenopiles commonly found in many freshwater, soil and marine environments. However, most research on Phytomyxea has been restricted to plant pathogenic species with agricultural importance, thereby missing the huge ecological potential of this enigmatic group of parasites. Members of the Phytomyxea can induce changes in biomass in their hosts (e.g. hypertrophies of the host tissue) under suitable environmental conditions. Upon infection they alter the metabolism of their hosts, consequently changing the metabolic status of their host. This results in an altered chemical composition of the host tissue, which impacts the diversity of species which feed on the tissues of the infected host and on the zoospores produced by the parasites. Furthermore, significant amounts of nutrients derived from the hosts, both primary producers (plants and algae) and primary consumers (litter decomposers and plant parasites [Oomycetes]), can enter the food web at different trophic levels in form of zoospores and resting spores. Large numbers of zoospores and resting spores are produced which can be eaten by secondary and tertiary consumers, such as grazing zooplankton and metazoan filter-feeders. Therefore, these microbes can act as energy-rich nutrient resources which may significantly alter the trophic relationships in fresh water, soil and marine habitats. Based on the presented data, Phytomyxea can significantly contribute to the complexity and energy transfer within food webs.     

Penetrability of the inner mucus layer: who is out there?

Large numbers of microorganisms colonise the skin and mucous membranes of animals, with their highest density in the lower gastrointestinal tract. The impact of these microbes on the host can be demonstrated by comparing animals (usually mice) housed under germ‐free conditions, or colonised with different compositions of microbes. Inbreeding and embryo manipulation programs have generated a wide variety of mouse strains with a fixed germ‐line (isogenic) and hygiene comparisons robustly show remarkably strong interactions between the microbiota and the host, which can be summarised in three axioms. (I) Live microbes are largely confined to their spaces at body surfaces, provided the animal is not suffering from an infection. (II) There is promiscuous molecular exchange throughout the host and its microbiota in both directions 1 . (III) Every host organ system is profoundly shaped by the presence of body surface microbes. It follows that one must draw a line between live microbial and host “spaces” (I) to understand the crosstalk (II and III) at this interesting interface of the host‐microbial superorganism. Of course, since microbes can adapt to very different niches, there has to be more than one line. In this issue of EMBO Reports, Johansson and colleagues have studied mucus, which is the main physical frontier for most microbes in the intestinal tract: they report how different non‐pathogenic microbiota compositions affect its permeability and the functional protection of the epithelial surface 2 .     

Moving targets: rapid evolution of oomycete effectors

Plant pathogenic microbes secrete proteins known as effectors, which enter the cytoplasm of plant cells and suppress host defences. Known effectors in oomycete pathogens possess an RXLR-EER motif in their amino acid sequence that is necessary for transport of the effector into a host plant cell. A large number of putative effectors have now been identified in oomycete genomes, the sequences of which show evidence of diversifying selection at their C terminus. Here, we describe recent progress in characterizing RXLR-EER effectors and discuss why so many of these rapidly evolving proteins are encoded by the genomes of plant pathogenic oomycetes.     

The Iron age of host–microbe interactions

Microbes exert a major impact on human health and disease by either promoting or disrupting homeostasis, in the latter instance leading to the development of infectious diseases. Such disparate outcomes are driven by the ever-evolving genetic diversity of microbes and the countervailing host responses that minimize their pathogenic impact. Host defense strategies that limit microbial pathogenicity include resistance mechanisms that exert a negative impact on microbes, and disease tolerance mechanisms that sustain host homeostasis without interfering directly with microbes. While genetically distinct, these host defense strategies are functionally integrated, via mechanisms that remain incompletely defined. Here, we explore the general principles via which host adaptive responses regulating iron (Fe) metabolism impact on resistance and disease tolerance to infection.     

Iron metabolism: microbes,mouse, and man

Recent advances in research on iron metabolism have revealed the identity of a number of genes, signal transduction pathways, and proteins involved in iron regulation in mammals. The emerging paradigm is a coordination of homeostasis within a network of classical iron metabolic pathways and other cellular processes such as cell differentiation, growth, inflammation, immunity, and a host of physiologic and pathologic conditions. Iron, immunity, and infection are intricately linked and their regulation is fundamental to the survival of mammals. The mutual dependence on iron by the host and invading pathogenic organisms elicits competition for the element during infection. While the host maintains mechanisms to utilize iron for its own metabolism exclusively, pathogenic organisms are armed with a myriad of strategies to circumvent these measures. This review explores iron metabolism in mammalian host, defense mechanisms against pathogenic microbes and the competitive devices of microbes for access to iron.     

Why bacteria matter in animal development and evolution

While largely studied because of their harmful effects on human health, there is growing appreciation that bacteria are important partners for invertebrates and vertebrates, including man. Epithelia in metazoans do not only select their microbiota; a coevolved consortium of microbes enables both invertebrates and vertebrates to expand the range of diet supply, to shape the complex immune system and to control pathogenic bacteria. Microbes in zebrafish and mice regulate gut epithelial homeostasis. In a squid, microbes control the development of the symbiotic light organ. These discoveries point to a key role for bacteria in any metazoan existence, and imply that beneficial bacteria‐host interactions should be considered an integral part of development and evolution.     

Beneficial microbes going underground of root immunity

Plant roots interact with an enormous diversity of commensal, mutualistic, and pathogenic microbes, which poses a big challenge to roots to distinguish beneficial microbes from harmful ones. Plants can effectively ward off pathogens following immune recognition of conserved microbe‐associated molecular patterns (MAMPs). However, such immune elicitors are essentially not different from those of neutral and beneficial microbes that are abundantly present in the root microbiome. Recent studies indicate that the plant immune system plays an active role in influencing rhizosphere microbiome composition. Moreover, it has become increasingly clear that root‐invading beneficial microbes, including rhizobia and arbuscular mycorrhiza, evade or suppress host immunity to establish a mutualistic relationship with their host. Evidence is accumulating that many free‐living rhizosphere microbiota members can suppress root immune responses, highlighting root immune suppression as an important function of the root microbiome. Thus, the gate keeping functions of the plant immune system are not restricted to warding off root‐invading pathogens but also extend to rhizosphere microbiota, likely to promote colonization by beneficial microbes and prevent growth‐defense tradeoffs triggered by the MAMP‐rich rhizosphere environment.     

Pathogenic chromatin modifiers: Their molecular action linking pathogenicity with genetic variability, epigenetic modifications and environmental factors in Alzheimer disease

Most Alzheimer disease (AD) cases are unexplained. To identify causative agents for AD and to understand this chronic, complex disease process, the pathogenic chromatin modification hypothesis is put forward here, which links pathogenicity with genetic variability, epigenetic modifications and environmental factors. Host chromatin modification by pathogens (disease producers) directly exploiting susceptible genes of their hosts with DNA cleavage, and DNA, histone and other host chromatin protein modifications at defined sites, provide an understanding of the molecular mechanisms for the gene variation associations for AD and the effect of environmental and epigenetic factors. With the pathogenic chromatin modification hypothesis, the erratic success for AD pathogenicity of certain microbes is explained. If a microbe contains the pathogenic chromatin modifiers or their genes, and has the opportunity to infect a host, which has gene variants vulnerable to the pathogenic chromatin modifiers, then the disease process is initiated and promoted. This hypothesis postulates that pathogenic chromatin modifiers contribute to the DNA damage found in AD, and are tied to known risks including the ?4 allele of apolipoprotein E, Down syndrome, the aging process and head injury. Restriction enzymes (REases) and methyltransferases (MTases), previously unrecognized as pathogens in AD or any disease, are a focus with specific suggestions for experiments to elucidate their possible role. The pathogenic chromatin modification hypothesis is relevant to other neurodegenerative disorders including human immunodeficiency virus (HIV) associated dementia and other chronic diseases. This work, integrating a multitude of genetic and environmental factors, presents new targets for therapeutic strategies.     

Soil microbes and the availability of soil nutrients

It is likely to provide plants with their necessary nutrients using chemical and biological fertilization. Although chemical fertilization is a quick method, it is not recommendable economically and environmentally, especially if overused. Biological fertilization is the use of soil microbes including arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria to inoculate plants. It has been proved that biological fertilization is an efficient method to supply plants with their necessary nutrients. It is economically and environmentally recommendable, because it results in sustainability. In this article, some of the most important details including the mechanisms and processes regarding the effects of soil microbes on the availability and hence uptake of nutrients by plant are reviewed. Such details can be important for the selection and hence production of microbial inoculums, which are appropriate for biological fertilization.     

植物与土壤微生物在调控生态系统养分循环中的作用

陆地生态系统的地上、地下是相互联系的。植物与土壤微生物作为陆地生态系统中的重要组成部分, 它们之间的相互作用是生态系统地上、地下结合的重要纽带。该文首先介绍了植物在养分循环中对营养元素的吸收、积累和归还等作用, 阐述了土壤微生物对养分有效性及土壤质量具有重要的作用。其次, 重点综述了植物与土壤微生物之间相互依存、相互竞争的关系。植物通过其凋落物与分泌物为土壤微生物提供营养, 土壤微生物作为分解者提供植物可吸收的营养元素, 比如共生体菌根真菌即可使植物根与土壤真菌达到互惠。然而, 植物的养分吸收与微生物的养分固持同时存在, 因而两者之间存在对养分的竞争。通过植物多样性对土壤微生物多样性的影响分析, 以及土壤微生物直接或间接作用于植物多样性和生产力的分析, 探讨了植物物种多样性与土壤微生物多样性之间的内在联系。针对当前植物与土壤微生物对养分循环的调控机制的争论, 提出植物凋落物是调节植物与土壤微生物养分循环的良好媒介, 植物与土壤微生物的共同作用对维持整个生态系统的稳定性具有重要意义。也指出了目前在陆地生态系统地上、地下研究中存在的不足和亟待解决的问题。     

RNA Splicing: A New Paradigm in Host–Pathogen Interactions

RNA splicing brings diversity to the eukaryotic proteome. Different spliced variants of a gene may differ in their structure, function, localization, and stability influencing protein stoichiometry and physiological outcomes. Alternate spliced variants of different genes are known to associate with various chronic pathologies including cancer. Emerging evidence suggests precise regulation of splicing as fundamental to normal well-being. In this context, infection-induced alternative splicing has emerged as a new pivot of host function, which pathogenic microbes can alter—directly or indirectly—to tweak the host immune responses against the pathogen. The implications of these findings are vast, and although not explored much in the case of pathogenic infections, we present here examples from splicing mediated regulation of immune responses across a variety of conditions and explore how this fascinating finding brings a new paradigm to host–pathogen interactions.     

抗生素对微生物作用的研究

抗生素能干扰微生物细胞新陈代谢的某个或几个环节 (包括代谢物或酶系统 ) ,使它不能以正常的代谢途径维持和延续生命活动。分别从抗生素抑制细胞壁合成、影响细胞膜功能、抑制蛋白质合成、影响能量代谢、干扰核酸合成 5方面综述了抗生素对微生物的作用。     

More than words: the chemistry behind the interactions in the plant holobiont

Plants and microbes have evolved sophisticated ways to communicate and coexist. The simplest interactions that occur in plant-associated habitats, i.e., those involved in disease detection, depend on the production of microbial pathogenic and virulence factors and the host's evolved immunological response. In contrast, microbes can also be beneficial for their host plants in a number of ways, including fighting pathogens and promoting plant growth. In order to clarify the mechanisms directly involved in these various plant–microbe interactions, we must still deepen our understanding of how these interkingdom communication systems, which are constantly modulated by resident microbial activity, are established and, most importantly, how their effects can span physically separated plant compartments. Efforts in this direction have revealed a complex and interconnected network of molecules and associated metabolic pathways that modulate plant–microbe and microbe–microbe communication pathways to regulate diverse ecological responses. Once sufficiently understood, these pathways will be biotechnologically exploitable, for example, in the use of beneficial microbes in sustainable agriculture. The aim of this review is to present the latest findings on the dazzlingly diverse arsenal of molecules that efficiently mediate specific microbe–microbe and microbe–plant communication pathways during plant development and on different plant organs.     

The contribution of melanin to microbial pathogenesis

Melanins are enigmatic pigments that are produced by a wide variety of microorganisms including several species of pathogenic bacteria, fungi and helminths. The study of melanin is difficult because these pigments defy complete biochemical and structural analysis. Nevertheless, the availability of new reagents in the form of monoclonal antibodies and melanin-binding peptides, combined with the application of various physical techniques, has provided insights into the process of melanization. Melanization is important in microbial pathogenesis because it has been associated with virulence in many microorganisms. Melanin appears to contribute to virulence by reducing the susceptibility of melanized microbes to host defence mechanisms. However, the interaction of melanized microbes and the host is complex and includes immune responses to melanin-related antigens. Production of melanin has also been linked to protection against environmental insults. Interference with melanization is a potential strategy for antimicrobial drug and pesticide development. The process of melanization poses fascinating problems in cell biology and provides a type of pathogenic strategy that is common to highly diverse pathogens.     

Scavenger receptors: role in innate immunity and microbial pathogenesis

Accumulating evidence shows that many scavenger receptors (SR), including SR-A, MARCO and CD36, represent an important part of the innate immune defence by acting as pattern-recognition receptors, in particular against bacterial pathogens. Several SR are expressed on macrophages and dendritic cells, where they act as phagocytic receptors mediating non-opsonic phagocytosis of pathogenic microbes. Another important function of some SR is to act as co-receptors to Toll-like receptors (TLR), modulating the inflammatory response to TLR agonists. On bacteria, the SR ligands have commonly been reported to be lipopolysaccharide and lipoteichoic acid, but recent advances in the field indicate that bacterial surface proteins play a more important role as target molecules for SR than previously thought. Interestingly, recent data show that major pathogens, including Streptococcus pyogenes and the group B streptococcus, have evolved mechanisms to evade SR-mediated recognition. Moreover, intracellular pathogens, such as hepatitis C virus and Plasmodium falciparum, utilize the SR to gain entry into host cells, focusing interest on the importance of SR also in the molecular pathogenesis of infectious diseases. This review highlights the complex interactions between SR and pathogenic microbes, and discusses the role of these interactions in host defence and microbial pathogenesis.     

植物寄生对生态系统结构和功能的影响

寄生植物是生态系统中的特殊类群之一。植物寄生可以驱动生态系统中生物与非生物因子的变化,在生态系统结构与功能中起关键作用。寄生植物可以通过对寄主营养的集聚、改变凋落物的质量与数量、改变根的周转与分泌物格局、改变土壤水势,从而影响土壤理化特性。寄生植物会改变寄主的行为,改变寄主与非寄主植物之间的相互作用,从而影响植物群落的结构、多样性和动态,进而影响植被演替和植被生产力等。寄生植物与寄主均可被消费者取食,可直接或间接地影响生态系统的食草动物,包括草食昆虫等。寄生植物与寄主的其它寄生物存在竞争关系,可以直接或间接地影响寄主的其它寄生植物或病原真菌。寄生植物可以明显地改变土壤地球化学循环,将固有的不可动的成分转变为可利用的营养成分,改变土壤生物群落的结构与功能,从而显著影响地下生物群落。这些表明,植物寄生对生态系统的结构和功能有重要影响。针对特殊的被入侵的植物群落,该地寄生植物可以通过影响入侵植物寄主的生长、繁殖、生物量分配格局,改变土壤的理化特性,促进非寄主的非优势本地植物的生长,从而改变被入侵植物群落结构与多样性,达到生物防治及生态恢复的目的。     

Immunity against extracellular pathogens

Summary Eukaryotic cells live in a relatively comfortable equilibrium with a wide variety of microbes. However, while many of the cohabiting microorganisms are harmless or even beneficial to the eukaryotic host, a number of prokaryotes have evolved the capacity to invade and replicate within host cells, thereby becoming potentially pathogenic. To be able to cope with potential pathogens, most organisms have developed several host defense mechanisms. First, microbes can be internalized and destroyed by a number of cell types of an innate immune system in a rather aspecific manner. Second, more complex organisms possess additionally an adaptive immune system that is capable of eliminating hazardous microbes in a highly specific manner. This review describes recent progress in our understanding of how pathogens interact with cells of the immune system, resulting in activation of the immune system or, for certain microorganisms, in the evasion of host defense reactions.     

Microbial Mechanisms of Heat Sensing

Temperature is one of the ubiquitous signals that control both the development as well as virulence of various microbial species. Therefore their survival is dependent upon initiating appropriate response upon temperature fluctuations. In particular, pathogenic microbes exploit host-temperature sensing mechanisms for triggering the expression of virulence genes. Many studies have revealed that the biomolecules within a cell such as DNA, RNA, lipids and proteins help in sensing change in temperature, thereby acting as thermosensors. This review shall provide an insight into the different mechanisms of thermosensing and how they aid pathogenic microbes in host invasion.