Photorhabdus: a model for the analysis of pathogenicity and mutualism

Photorhabdus are entomopathogenic members of the family Enterobacteriaceae. In addition to killing insects Photorhabdus also have a mutualistic association with nematodes from the family Heterorhabditidiae. Therefore, the bacteria have a complex life cycle that involves temporally separated pathogenic and mutualistic associations with two different invertebrate hosts. This tripartite Photorhabdus-insect-nematode association provides researchers with a unique opportunity to characterize the prokaryotic contribution to two different symbioses, i.e. pathogenicity and mutualism while also studying the role of the host in determining the outcome of association with the bacteria. In this review I will outline the life cycle of Photorhabdus and describe recent important advances in our understanding of the symbiology of Photorhabdus. Finally, the contribution made by this model to our understanding of the nature of symbiotic associations will be discussed.     

A model for endosymbiosis: Interaction between Tetrahymena pyriformis and Escherichia coli

Endosymbiosis in ciliates is a common and highly diverse phenomenon in nature, but its development at the mechanistic level and the origins are not easy to understand, since these associations may have arisen at any time during evolution. Therefore a laboratory model is helpful. It could be provided by the interaction of Tetrahymena pyriformis and Escherichia coli. Microscopic analyses with a genetically manipulated fluorescent strain of E. coli show single bacteria leaving food vacuoles and escaping digestion, an important prerequisite for further experiments. Under selective conditions, beneficial for T. pyriformis, the ciliate was shown to internalize E. coli cells. After feeding, bacteria, transformed with the plasmids pBS-neoTet or pNeo4, provide T. pyriformis with the ability to handle toxic conditions, caused by the aminoglykoside antibiotic paromomycin. Axenic cultures or cocultures with untransformed bacteria show lower cell numbers and survival rates compared to cocultures with transformed bacteria after transfer to paromomycin containing media. PCR detects bacterial DNA inside T. pyriformis cells. Additionally, microscopical analysis of selectively grown cocultures reveals fluorescing particles in the cytoplasm of T. pyriformis containing DNA and lipids, corresponding in size to E. coli. This system could be a reasonable model for understanding mechanisms of endosymbiosis establishment in ciliates.     

Effects of a belowground mutualism on an aboveground mutualism

Studies of multitrophic interactions between below‐ and aboveground communities have generally focused on soil organisms and antagonists of plant shoots and leaves (herbivores). Despite the widespread occurrence of plant mutualists below‐ and aboveground which can occur on the same host plant, the potential for interactions between them has not been considered. Here we demonstrate that aboveground plant mutualists, insect pollinators, are strongly influenced by belowground plant mutualists, arbuscular mycorrhizal fungi. The presence of arbuscular mycorrhizal fungi in the roots of Chamerion angustifolium increased pollinator visitation and per cent seed set of this plant in the field by up to two times compared with non‐mycorrhizal plants. We propose that interactions between belowground and aboveground mutualisms are widespread and may play important functional roles in populations and communities.     

Back to primary endosymbiosis: from plastids to artificial photosynthetic life-forms

Throughout evolution, only two known primary photosynthetic endosymbiosis occurred, which originated the Archaeplastida and the Paulinella spp. Fundamental questions regarding primary endosymbiosis remain unsolved, but may now be addressed with the recent development of chimeric photosynthetic life-form. Cournoyer et al. could establish artificial photosynthetic endosymbiosis between yeast and cyanobacteria.     

Nematode–bacteria mutualism: Selection within the mutualism supersedes selection outside of the mutualism

The coevolution of interacting species can lead to codependent mutualists. Little is known about the effect of selection on partners within verses apart from the association. Here, we determined the effect of selection on bacteria (Xenorhabdus nematophila) both within and apart from its mutualistic partner (a nematode, Steinernema carpocapsae). In nature, the two species cooperatively infect and kill arthropods. We passaged the bacteria either together with (M+), or isolated from (M?), nematodes under two different selection regimes: random selection (S?) and selection for increased virulence against arthropod hosts (S+). We found that the isolated bacteria evolved greater virulence under selection for greater virulence (M?S+) than under random selection (M?S?). In addition, the response to selection in the isolated bacteria (M?S+) caused a breakdown of the mutualism following reintroduction to the nematode. Finally, selection for greater virulence did not alter the evolutionary trajectories of bacteria passaged within the mutualism (M+S+ = M+S?), indicating that selection for the maintenance of the mutualism was stronger than selection for increased virulence. The results show that selection on isolated mutualists can rapidly breakdown beneficial interactions between species, but that selection within a mutualism can supersede external selection, potentially generating codependence over time.     

Cheating on a mutualism: indirect benefits of ant attendance to a coccidophagous coccinellid

Coccinellids (Coleoptera: Coccinellidae) are generally unable to prey on ant-tended prey. However, particular coccinellid species have morphological, behavioral, or chemical characteristics that render them immune to ant attacks, and some species are even restricted to ant-tending areas. The benefit gained from living in close association with ants can be twofold: (1) gaining access to high-density prey areas and (2) gaining enemy-free space. Here, the myrmecophily of Azya orbigera Mulsant (Coleoptera: Coccinellidae), an important predator of the green coffee scale, Coccus viridis (Green) (Hemiptera: Coccidae), is reported. In this paper, three main questions were studied. (1) Are the waxy filaments of A. orbigera larvae effective as defense against attacks of the mutualistic ant partner of C. viridis, Azteca instabilis F. Smith (Hymenoptera: Formicidae)? (2) Does A. instabilis reduce the rate at which A. orbigera larvae prey on scales? (3) Do A. orbigera larvae gain enemy-free space by living in close association with A. instabilis? Laboratory and field experiments were conducted to answer these questions. We found that, because of the sticky waxy filaments of A. orbigera larvae, A. instabilis is incapable of effectively attacking them and, therefore, the predation rate of A. orbigera on C. viridis does not decrease in the presence of ants. Furthermore, A. instabilis showed aggressive behavior toward A. orbigera's parasitoids, and the presence of ants reduced the parasitism suffered by A. orbigera. This is the first time that this kind of indirect positive effect is reported for an ant and a coccidophagous coccinellid. Furthermore, this indirect positive effect may be key to the persistence of A. orbigera's populations.     

A plastid in the making: evidence for a second primary endosymbiosis

One of the major steps in the evolution of life was the origin of photosynthesis in nucleated cells underpinning the evolution of plants. It is well accepted that this evolutionary process was initiated when a photosynthetic bacterium (a cyanobacterium) was taken up by a colorless host cell, probably more than a billion years ago, and transformed into a photosynthetic organelle (a plastid) during a process known as primary endosymbiosis. Here, we use sequence comparisons and phylogenetic analyses of the prokaryotic rDNA operon to show that the thecate, filose amoeba Paulinella chromatophora Lauterborn obtained its photosynthetic organelles by a similar but more recent process, which involved a different cyanobacterium, indicating that the evolution of photosynthetic organelles from cyanobacteria was not a unique event, as is commonly believed, but may be an ongoing process.     

A mathematical model of facultative mutualism with populations interacting in a food chain

Facultative mutualism with populations interacting in a food chain is modeled by a system of four autonomous ordinary differential equations. Two cases are considered: mutualism with the prey and mutualism with the first predator. In both cases persistence and extinction criteria are developed in terms of the invariant flows on the boundaries.     

Algal genomics: exploring the imprint of endosymbiosis

The nuclear genomes of photosynthetic eukaryotes are littered with genes derived from the cyanobacterial progenitor of modern-day plastids. A genomic analysis of Cyanophora paradoxa - a deeply diverged unicellular alga - suggests that the abundance and functional diversity of nucleus-encoded genes of cyanobacterial origin differs in plants and algae.     

Dynamics within mutualism and the maintenance of diversity: inference from a model of interguild frequency dependence

Numerical models have suggested that the dynamics within mutualisms are not important for the maintenance of diversity. In this study it is demonstrated that the dynamics within mutualism can contribute to the maintenance of diversity within its participants, using a general model of frequency dependence between two mutualistically interacting guilds. Specifically, it is demonstrated that while mutualisms may exhibit positive feedback in density, there may be a negative feedback within a mutualism as a result of the change in composition within the interacting guild. Such a negative feedback results from an asymmetry in the delivery of benefit between participants of the mutualism that generates a negative interguild frequency dependence. This dynamic contributes to the maintenance of diversity within the interacting guilds. Conditions are identified for the maintenance of diversity and the maximization of benefit from mutualism within the context of the model. The utility of these conditions for testing hypotheses using data from the mutualistic interaction between plants and mycorrhizal fungi is then demonstrated.     

WBE 模型及其在生态学中的应用：研究概述

介绍了WBE模型,综述了该模型在生态学中的应用进展。WBE模型,以及以该模型为基础的MTE模型,假设生物体为自相似分形网络结构,提出代谢速率和个体大小之间存在3/4指数关系,分别预测了从个体到生物圈多个尺度上的生物属性之间的异速生长关系,而且部分得到了验证。WBE模型的应用涵盖了个体组织生物量、年生长率,种群密度和生态系统单位面积产量、能量流动率等多个方面;即使在生物圈大尺度上,WBE模型也可用来预测试验中无法直接测量的特征变量的属性,如全球碳储量的估算等。至今,关于WBE和MTE模型仍然存在各种褒贬争论,讨论焦点主要集中于模型建立的前提假设以及权度指数的预测。今后的研究工作应规范试验技术和方法,考虑物种多样性和环境等因素的影响,提出符合各类生物的模型结构体系,使其具有更广泛的应用性和预测性。     

Review: origin of complex algae by secondary endosymbiosis: a journey through time

Secondary endosymbiosis—the merging of two eukaryotic cells into one photosynthetic cellular unit—led to the evolution of ecologically and medically very important organisms. We review the biology of these organisms, starting from the first proposal of secondary endosymbiosis up to recent phylogenetic models on the origin of secondarily evolved protists. In addition, we discuss the organelle character of the symbionts based on morphological features, gene transfers from the symbiont into the host and re-import of nucleus-encoded plastid proteins. Finally, we hypothesize that secondary endosymbiosis is more than enslaving a eukaryotic, phototrophic cell, but reflects a complex interplay between host and symbiont, leading to the inseparability of the two symbiotic partners generating a cellular entity.     

Optimal resource allocation model for excessive flower production in a pollinating seed-predator mutualism

Many plants produce excessive flowers and several hypotheses have been proposed for adaptive significances of this behavior. Here, I develop a simple resource allocation model for plants in a mutualism with pollinating seed-predators to examine a novel hypothesis that excessive flower production can be favored to “dilute” seed predation by the pollinators. Pollinators visit flowers to deposit pollen and oviposit on them, and their offspring feed on a portion of the seeds, leaving the remainder intact. Further pollinator visits increase seed mortality by over-oviposition. Excessive flower production is favored if it decreases pollinator-visit frequency per flower, while it incurs decrease in seed production because of the resource trade-off. I examine three plant strategies: (1) no abortion, the plant allocates resource to all pollinated flowers to mature; (2) selective abortion, the plant aborts flowers depending on how many times they were visited by pollinators; and (3) random abortion, the plant indiscriminately aborts a fraction of pollinated flowers irrespective of how many times they were visited. I show that the random abortion strategy can perform much more effectively than the no-abortion strategy when the amount of resource is small, the production cost per flower is low, and the pollinator density is high, although the selective abortion strategy is always the best. This “predator dilution” effect has not been considered with regard to previous excessive flower production hypotheses.