Chemical signals driving bacterial–fungal interactions

Microorganisms reside in diverse environmental communities where interactions become indispensable due to close physical associations. These interactions are driven by chemical communication among different microbial kingdoms, particularly between fungi and bacteria. Knowledge about these communication signals provides useful information about the nature of microbial interactions and allows predictions of community development in diverse environments. Here, we provide an update on the role of small signalling molecules in fungal–bacterial interactions with focus on agricultural and medicinal environments. This review highlights the range of – and response to – diverse biochemicals produced by both kingdoms with view to harnessing their properties towards drug discovery applications.     

The chemical defense ecology of marine unicellular plankton: constraints, mechanisms, and impacts

The activities of unicellular microbes dominate the ecology of the marine environment, but the chemical signals that determine behavioral interactions are poorly known. In particular, chemical signals between microbial predators and prey contribute to food selection or avoidance and to defense, factors that probably affect trophic structure and such large-scale features as algal blooms. Using defense as an example, I consider physical constraints on the transmission of chemical information, and strategies and mechanisms that microbes might use to send chemical signals. Chemical signals in a low Re, viscosity-dominated physical environment are transferred by molecular diffusion and laminar advection, and may be perceived at nanomolar levels or lower. Events that occur on small temporal and physical scales in the "near-field" of prey are likely to play a role in cell-cell interactions. On the basis of cost-benefit optimization and the need for rapid activation, I suggest that microbial defense system strategies might be highly dynamic. These strategies include compartmented and activated reactions, utilizing both pulsed release of dissolved signals and contact-activated signals at the cell surface. Bioluminescence and extrusome discharge are two visible manifestations of rapidly activated microbial defenses that may serve as models for other chemical reactions as yet undetected due to the technical problems of measuring transient chemical gradients around single cells. As an example, I detail an algal dimethylsulfoniopropionate (DMSP) cleavage reaction that appears to deter protozoan feeding and explore it as a possible model for a rapidly activated, short-range chemical defense system. Although the exploration of chemical interactions among planktonic microbes is in its infancy, ecological models from macroorganisms provide useful hints of the complexity likely to be found.     

Inter-plant vibrational communication in a leafhopper insect

Vibrational communication is one of the least understood channels of communication. Most studies have focused on the role of substrate-borne signals in insect mating behavior, where a male and a female establish a stereotyped duet that enables partner recognition and localization. While the effective communication range of substrate-borne signals may be up to several meters, it is generally accepted that insect vibrational communication is limited to a continuous substrate. Until now, interplant communication in absence of physical contact between plants has never been demonstrated in a vibrational communicating insect. With a laser vibrometer we investigated transmission of natural and played back vibrational signals of a grapevine leafhopper, Scaphoideus titanus, when being transmitted between leaves of different cuttings without physical contact. Partners established a vibrational duet up to 6 cm gap width between leaves. Ablation of the antennae showed that antennal mechanoreceptors are not essential in detection of mating signals. Our results demonstrate for the first time that substrate discontinuity does not impose a limitation on communication range of vibrational signals. We also suggest that the behavioral response may depend on the signal intensity.     

Information,influence, and the causal-explanatory role of content in understanding receiver responses

Sceptics of informational terminology argue that by attributing content to signals, we fail to address nonhuman animal communication on its own terms. Primarily, we ignore that communication is sender driven: i.e. driven by the intrinsic physical properties of signals, themselves the result of selection pressures acting on signals to influence receivers in ways beneficial for senders. In contrast, information proponents argue that this ignores the degree to which communication is, in fact, receiver driven. The latter argue that an exclusive focus on the intrinsic mechanical properties of signals cannot explain why receivers respond as they do. This is because receivers are not prisoners of sender influence. They possess response flexibility, and so we can only explain why receivers respond to signals as they do by positing that receivers ‘derive information’ from signals. I argue that, while basically true, this response flexibility can take one of two forms depending on the causal-explanatory role of information in understanding the response of the receiver: diachronic, on the one hand; and synchronic, on the other. In species with diachronic response flexibility only, information is derived by receivers from signals in a minimal sense. In such cases, information is an ultimate explanatory construct: one underpinned by historical facts at the population level. Alternatively, in species with synchronic response flexibility, information is derived by receivers from signals in a richer sense. Here, information is a proximate explanatory construct: one underpinned by cognitive-mechanistic facts at the level of the individual organism. Without recognising the different ways information can be derived from signals, and the different causal-explanatory roles (ultimate vs proximate) information can play in understanding alternate kinds of receiver flexibility (diachronic vs synchronic), proponents of information leave themselves open to the charge of anthropomorphising some signalling systems.     

Mechanisms of biofilm resistance to antimicrobial agents

Biofilms are communities of microorganisms attached to a surface. It has become clear that biofilm-grown cells express properties distinct from planktonic cells, one of which is an increased resistance to antimicrobial agents. Recent work has indicated that slow growth and/or induction of an rpoS-mediated stress response could contribute to biocide resistance. The physical and/or chemical structure of exopolysaccharides or other aspects of biofilm architecture could also confer resistance by exclusion of biocides from the bacterial community. Finally, biofilm-grown bacteria might develop a biofilm-specific biocide-resistant phenotype. Owing to the heterogeneous nature of the biofilm, it is likely that there are multiple resistance mechanisms at work within a single community. Recent research has begun to shed light on how and why surface-attached microbial communities develop resistance to antimicrobial agents.     

Communication in bacteria: an ecological and evolutionary perspective

Individual bacteria can alter their behaviour through chemical interactions between organisms in microbial communities - this is generally referred to as quorum sensing. Frequently, these interactions are interpreted in terms of communication to mediate coordinated, multicellular behaviour. We show that the nature of interactions through quorum-sensing chemicals does not simply involve cooperative signals, but entails other interactions such as cues and chemical manipulations. These signals might have a role in conflicts within and between species. The nature of the chemical interaction is important to take into account when studying why and how bacteria react to the chemical substances that are produced by other bacteria.     

Synthesizing traditional biogeography with microbial ecology: the importance of dormancy

The discovery of biogeographical patterns among microbial communities has led to a focus on the empirical evaluation of the importance of dispersal limitation in microbial biota. As a result, the spatial distribution of microbial diversity has been increasingly studied while the synthesis of biogeographical theory with microbial ecology remains undeveloped. To make biogeographical theory relevant to microbial ecology, microbial traits that potentially affect the distribution of microbial diversity need to be considered. Given that many microorganisms in natural environments are in a state of dormancy and that dormancy is an important microbial fitness trait, I provide a first attempt to account for the effects of dormancy on microbial biogeography by treating dormancy as a fundamental biogeographical response. I discuss the effects of dormancy on the equilibrium theory of island biogeography and on the unified neutral theory of biodiversity and biogeography, and suggest how the equilibrium theory of island biogeography can produce predictions approaching those of the Baas‐Becking hypothesis (i.e. everything is everywhere, but the environment selects). In addition, I present a conceptual model of the unified neutral theory of biodiversity and biogeography, generalized to account for dormancy, from which a full model can be constructed for species with or without dormant life history stages.     

Electrogenetic signaling and information propagation for controlling microbial consortia via programmed lysis

To probe signal propagation and genetic actuation in microbial consortia, we have coopted the components of both redox and quorum sensing (QS) signaling into a communication network for guiding composition by “programming” cell lysis. Here, we use an electrode to generate hydrogen peroxide as a redox cue that determines consortia composition. The oxidative stress regulon of Escherichia coli, OxyR, is employed to receive and transform this signal into a QS signal that coordinates the lysis of a subpopulation of cells. We examine a suite of information transfer modalities including “monoculture” and “transmitter-receiver” models, as well as a series of genetic circuits that introduce time-delays for altering information relay, thereby expanding design space. A simple mathematical model aids in developing communication schemes that accommodate the transient nature of redox signals and the “collective” attributes of QS signals. We suggest this platform methodology will be useful in understanding and controlling synthetic microbial consortia for a variety of applications, including biomanufacturing and biocontainment.     

Evolutionary conditions for the emergence of communication in robots

Information transfer plays a central role in the biology of most organisms, particularly social species [1, 2]. Although the neurophysiological processes by which signals are produced, conducted, perceived, and interpreted are well understood, the conditions conducive to the evolution of communication and the paths by which reliable systems of communication become established remain largely unknown. This is a particularly challenging problem because efficient communication requires tight coevolution between the signal emitted and the response elicited [3]. We conducted repeated trials of experimental evolution with robots that could produce visual signals to provide information on food location. We found that communication readily evolves when colonies consist of genetically similar individuals and when selection acts at the colony level. We identified several distinct communication systems that differed in their efficiency. Once a given system of communication was well established, it constrained the evolution of more efficient communication systems. Under individual selection, the ability to produce visual signals resulted in the evolution of deceptive communication strategies in colonies of unrelated robots and a concomitant decrease in colony performance. This study generates predictions about the evolutionary conditions conducive to the emergence of communication and provides guidelines for designing artificial evolutionary systems displaying spontaneous communication.     

Coevolution of visual signals and eye morphology in Polistes paper wasps

To be effective, signals must propagate through the environment and be detected by receivers. As a result, signal form evolves in response to both the constraints imposed by the transmission environment and receiver perceptual abilities. Little work has examined the extent to which signals may act as selective forces on receiver sensory systems to improve the efficacy of communication. If receivers benefit from accurate signal assessment, selection could favour sensory organs that improve discrimination of established signals. Here, we provide evidence that visual resolution coevolves with visual signals in Polistes wasps. Multiple Polistes species have variable facial patterns that function as social signals, whereas other species lack visual signals. Analysis of 19 Polistes species shows that maximum eye facet size is positively associated with both eye size and presence of visual signals. Relatively larger facets within the eye''s acute zone improve resolution of small images, such as wasp facial signals. Therefore, sensory systems may evolve to optimize signal assessment. Sensory adaptations to facilitate signal detection may represent an overlooked area of the evolution of animal communication.     

Do aggressive signals evolve towards higher reliability or lower costs of assessment?

It has been suggested that the evolution of signals must be a wasteful process for the signaller, aimed at the maximization of signal honesty. However, the reliability of communication depends not only on the costs paid by signallers but also on the costs paid by receivers during assessment, and less attention has been given to the interaction between these two types of costs during the evolution of signalling systems. A signaller and receiver may accept some level of signal dishonesty by choosing signals that are cheaper in terms of assessment but that are stabilized with less reliable mechanisms. I studied the potential trade‐off between signal reliability and the costs of signal assessment in the corncrake (Crex crex). I found that the birds prefer signals that are less costly regarding assessment rather than more reliable. Despite the fact that the fundamental frequency of calls was a strong predictor of male size, it was ignored by receivers unless they could directly compare signal variants. My data revealed a response advantage of costly signals when comparison between calls differing with fundamental frequencies is fast and straightforward, whereas cheap signalling is preferred in natural conditions. These data might improve our understanding of the influence of receivers on signal design because they support the hypothesis that fully honest signalling systems may be prone to dishonesty based on the effects of receiver costs and be replaced by signals that are cheaper in production and reception but more susceptible to cheating.     

Differential signal sensitivities can contribute to the stability of multispecies bacterial communities

Background

Bacterial species present in multispecies microbial communities often react to the same chemical signal but at vastly different concentrations. The existence of different response thresholds with respect to the same signal molecule has been well documented in quorum sensing which is one of the best studied inter-cellular signalling mechanisms in bacteria. The biological significance of this phenomenon is still poorly understood, and cannot be easily studied in nature or in laboratory models. The aim of this study is to establish the role of differential signal response thresholds in stabilizing microbial communities.

Results

We tested binary competition scenarios using an agent-based model in which competing bacteria had different response levels with respect to signals, cooperation factors or both, respectively. While in previous scenarios fitter species outcompete slower growing competitors, we found that stable equilibria could form if the fitter species responded to a higher chemical concentration level than the slower growing competitor. We also found that species secreting antibiotic could form a stable community with other competing species if antibiotic production started at higher response thresholds.

Conclusions

Microbial communities in nature rely on the stable coexistence of species that necessarily differ in their fitness. We found that differential response thresholds provide a simple and elegant way for keeping slower growing species within the community. High response thresholds can be considered as self-restraint of the fitter species that allows metabolically useful but slower growing species to remain within a community, and thereby the metabolic repertoire of the community will be maintained.

Reviewers

This article was reviewed by Michael Gromiha, Sebastian Maurer-Stroh, István Simon and L. Aravind.

     

Computer-generated animal model stimuli

Communication between animals is diverse and complex. Animals may communicate using auditory, seismic, chemosensory, electrical, or visual signals. In particular, understanding the constraints on visual signal design for communication has been of great interest. Traditional methods for investigating animal interactions have used basic observational techniques, staged encounters, or physical manipulation of morphology. Less intrusive methods have tried to simulate conspecifics using crude playback tools, such as mirrors, still images, or models. As technology has become more advanced, video playback has emerged as another tool in which to examine visual communication (Rosenthal, 2000). However, to move one step further, the application of computer-animation now allows researchers to specifically isolate critical components necessary to elicit social responses from conspecifics, and manipulate these features to control interactions. Here, I provide detail on how to create an animation using the Jacky dragon as a model, but this process may be adaptable for other species. In building the animation, I elected to use Lightwave 3D to alter object morphology, add texture, install bones, and provide comparable weight shading that prevents exaggerated movement. The animation is then matched to select motor patterns to replicate critical movement features. Finally, the sequence must rendered into an individual clip for presentation. Although there are other adaptable techniques, this particular method had been demonstrated to be effective in eliciting both conspicuous and social responses in staged interactions.     

Toward an understanding of microbial communities through analysis of communication networks

Bacteria receive signals from diverse members of their biotic environment. They sense their own species through the process of quorum sensing, which detects the density of bacterial cells and regulates functions such as bioluminescence, virulence, and competence. Bacteria also respond to the presence of other microorganisms and eukaryotic hosts. Most studies of microbial communication focus on signaling between the microbe and one other organism for empirical simplicity and because few experimental systems offer the opportunity to study communication among various types of organisms. But in the real biological world, microorganisms must carry on multiple molecular conversations simultaneously between diverse organisms, thereby constructing communication networks. We propose that biocontrol of plant disease, the process of suppressing disease through application of a microorganism, offers a model for the study of communication among multiple organisms. Successful biocontrol requires the sending and receiving of signals between the biocontrol agent and the pathogen, plant host, and microbial community surrounding the host. We are using Bacillus cereus, a biocontrol agent, and the organisms it must interact with, to dissect a communication network. This system offers an excellent starting point for study because its members are defined and well studied. An understanding of signaling in the B. cereus biocontrol system may provide a model for network communication among organisms that share a habitat and provide a new angle of analysis for understanding the interconnections that define communities. This revised version was published online in August 2006 with corrections to the Cover Date.     

The enzymes of bacterial census and censorship

N-Acyl-L-homoserine lactones (AHLs) are a major class of quorum-sensing signals used by Gram-negative bacteria to regulate gene expression in a population-dependent manner, thereby enabling group behavior. Enzymes capable of generating and catabolizing AHL signals are of significant interest for the study of microbial ecology and quorum-sensing pathways, for understanding the systems that bacteria have evolved to interact with small-molecule signals, and for their possible use in therapeutic and industrial applications. The recent structural and functional studies reviewed here provide a detailed insight into the chemistry and enzymology of bacterial communication.     

Tremulatory and Abdomen Vibration Signals Enable Communication through Air in the Stink Bug Euschistus heros

Communication by substrate-borne mechanical signals is widespread among animals but remains one of their least understood communication channels. Past studies of vibrational communication in insects have been oriented predominantly to communication during mating, showing that species- and sex-specific vibrational signals enable recognition and localization of potential mates on continuous solid substrates. No special attention has been paid to vibrational signals with less obvious specificity as well as to the possibility of vibrational communication across substrates that are not in physical contact. We aimed to reinvestigate emission of the aforementioned vibrational signals transmitted through a plant in the stink bug Euschistus heros (Pentatomidae: Pentatominae) and to check whether individuals are able to communicate across adjecent, physically separated substrates. We used laser vibrometry for registration of substrate-borne vibrational signals on a bean plant. Using two bean plants separated for 3 to 7 cm between two most adjacent leaves, we investigated the possibility of transmission of these signals through air. Our study showed that males and females of E. heros communicate using tremulatory, percussion and buzzing signals in addition to the previously described signals produced by vibrations of the abdomen. Contrary to the latter, the first three signal types did not differ between sexes or between pentatomid species. Experiments with two physically separated plants showed significant searching behaviour and localization of vibrational signals of an E. heros male or a female, in response to abdominal vibration produced signals of a pair duetting on the neighbouring plant, in comparison to control where no animals were on the neighbouring plant. We also confirmed that transmission through air causes amplitude and frequency decay of vibrational signals, which suggests high-amplitude, low-frequency tremulatory signals of these stink bugs their most plausible way of communication across discontinuous substrates.     

Functionally referential signals: A promising paradigm whose time has passed

Finding the evolutionary origins of human language in the communication systems of our closest living relatives has, for the last several decades, been a major goal of many in the field of animal communication generally and primate communication specifically. 1 - 4 The so‐called “functionally referential” signals have long been considered promising in this regard, with apparent parallels with the semantic communication that characterizes language. The once‐prominent idea that functionally referential signals are word‐like, in that they are arbitrary sounds that refer to phenomena external to the caller, has largely been abandoned. 5 However, the idea that these signals may offer the strongest link between primate communication and human language remains widespread, primarily due to the fact the behavior of receivers indicates that such signals enable them to make very specific inferences about their physical or social environment. Here we review the concept of functional reference and discuss modern perspectives that indicate that, although the sophistication of receivers provides some continuity between nonhuman primate and human cognition, this continuity is not unique to functionally referential signals. In fact, because functionally referential signals are, by definition, produced only in specific contexts, receivers are less dependent on the integration of contextual cues with signal features to determine an appropriate response. The processing of functionally referential signals is therefore likely to entail simpler cognitive operations than does that of less context‐specific signals. While studies of functional reference have been important in highlighting the relatively sophisticated processes that underlie receiver behavior, we believe that the continued focus on context‐specific calls detracts from the potentially more complex processes underlying responses to more unspecific calls. In this sense, we argue that the concept of functional reference, while historically important for the field, has outlived its usefulness and become a red herring in the pursuit of the links between primate communication and human language. © 2012 Wiley Periodicals, Inc.     

From Sender to Receiver: Propagation and Environmental Effects on Acoustic Signals

SYNOPSIS. Acoustic signals transmitted over large distancesdiffer significantly from those emitted by the signaler. Acousticsignals degrade in amplitude, spectral and temporal structureas they propagate through theenvironment. A great deal of workon acoustic communication is aimed at understanding the selectiveforces imposed by the environment on animal signals. I willdiscuss the physical constraints the environment puts on acousticcommunication, and then discuss similarities in communicationby anurans and insects that relate these environmental constraintsto their signaling systems. Lastly, I show how changes in signalsduring propagation relate to changes in signal perception duringphonotaxis, and thus, how propagation relates to mate choiceand sexual selection     

A sense of danger from radiation

Tissue damage caused by exposure to pathogens, chemicals and physical agents such as ionizing radiation triggers production of generic "danger" signals that mobilize the innate and acquired immune system to deal with the intrusion and effect tissue repair with the goal of maintaining the integrity of the tissue and the body. Ionizing radiation appears to do the same, but less is known about the role of "danger" signals in tissue responses to this agent. This review deals with the nature of putative "danger" signals that may be generated by exposure to ionizing radiation and their significance. There are a number of potential consequences of "danger" signaling in response to radiation exposure. "Danger" signals could mediate the pathogenesis of, or recovery from, radiation damage. They could alter intrinsic cellular radiosensitivity or initiate radioadaptive responses to subsequent exposure. They may spread outside the locally damaged site and mediate bystander or "out-of-field" radiation effects. Finally, an important aspect of classical "danger" signals is that they link initial nonspecific immune responses in a pathological site to the development of specific adaptive immunity. Interestingly, in the case of radiation, there is little evidence that "danger" signals efficiently translate radiation-induced tumor cell death into the generation of tumor-specific immunity or normal tissue damage into autoimmunity. The suggestion is that radiation-induced "danger" signals may be inadequate in this respect or that radiation interferes with the generation of specific immunity. There are many issues that need to be resolved regarding "danger" signaling after exposure to ionizing radiation. Evidence of their importance is, in some areas, scant, but the issues are worthy of consideration, if for no other reason than that manipulation of these pathways has the potential to improve the therapeutic benefit of radiation therapy. This article focuses on how normal tissues and tumors sense and respond to danger from ionizing radiation, on the nature of the signals that are sent, and on the impact on the eventual consequences of exposure.     

Communication among Oral Bacteria

Human oral bacteria interact with their environment by attaching to surfaces and establishing mixed-species communities. As each bacterial cell attaches, it forms a new surface to which other cells can adhere. Adherence and community development are spatiotemporal; such order requires communication. The discovery of soluble signals, such as autoinducer-2, that may be exchanged within multispecies communities to convey information between organisms has emerged as a new research direction. Direct-contact signals, such as adhesins and receptors, that elicit changes in gene expression after cell-cell contact and biofilm growth are also an active research area. Considering that the majority of oral bacteria are organized in dense three-dimensional biofilms on teeth, confocal microscopy and fluorescently labeled probes provide valuable approaches for investigating the architecture of these organized communities in situ. Oral biofilms are readily accessible to microbiologists and are excellent model systems for studies of microbial communication. One attractive model system is a saliva-coated flowcell with oral bacterial biofilms growing on saliva as the sole nutrient source; an intergeneric mutualism is discussed. Several oral bacterial species are amenable to genetic manipulation for molecular characterization of communication both among bacteria and between bacteria and the host. A successful search for genes critical for mixed-species community organization will be accomplished only when it is conducted with mixed-species communities.