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.     

Wild Western Lowland Gorillas Signal Selectively Using Odor

Mammals communicate socially through visual, auditory and chemical signals. The chemical sense is the oldest sense and is shared by all organisms including bacteria. Despite mounting evidence for social chemo-signaling in humans, the extent to which it modulates behavior is debated and can benefit from comparative models of closely related hominoids. The use of odor cues in wild ape social communication has been only rarely explored. Apart from one study on wild chimpanzee sniffing, our understanding is limited to anecdotes. We present the first study of wild gorilla chemo-communication and the first analysis of olfactory signaling in relation to arousal levels and odor strength in wild apes. If gorilla scent is used as a signaling mechanism instead of only a sign of arousal or stress, odor emission should be context specific and capable of variation as a function of the relationships between the emitter and perceiver(s). Measured through a human pungency scale, we determined the factors that predicted extreme levels of silverback odor for one wild western lowland gorilla (Gorilla gorilla gorilla) group silverback. Extreme silverback odor was predicted by the presence and intensity of inter-unit interactions, silverback anger, distress and long-calling auditory rates, and the absence of close proximity between the silverback and mother of the youngest infant. Odor strength also varied according to the focal silverback''s strategic responses during high intensity inter-unit interactions. Silverbacks appear to use odor as a modifiable form of communication; where odor acts as a highly flexible, context dependent signaling mechanism to group members and extra-group units. The importance of olfaction to ape social communication may be especially pertinent in Central African forests where limited visibility may necessitate increased reliance on other senses.     

Group chorusing as an intragroup signal in the greater ani,a communally breeding bird

Group living often requires maintaining dynamic and varied relationships with fellow group members, while simultaneously monitoring and interacting with external competitors. Group members in many social species vocalize together to produce duets or choruses—coordinated, often conspicuous vocal displays—that may play a role in these interactions. Compared with male–female duets, however, relatively little research exists on the function and adaptive significance of group choruses, which involve three or more individuals. Here we investigate chorusing behavior in the greater ani (Crotophaga major), a communally breeding cuckoo that nests in stable social groups of four to eight unrelated individuals. Groups may remain together for several years on the same nesting territory, and groups occasionally destroy each other's clutches in conflicts over high-quality territories. We asked whether the raucous, highly stereotyped choruses performed by ani groups are primarily used for intra- or intergroup communication, and whether they contain information about the identity of the social group and the number of birds vocalizing. Behavioral observations and acoustic recordings from three breeding seasons revealed that choruses typically occurred during social interactions within the group (78% of choruses) or in response to a predator or extra-group individual (17%) and only rarely in intergroup interactions (4%). Consistent with this finding, choruses did not reliably reflect the number of birds vocalizing, and we found only limited evidence for group-specific acoustic signatures (driven by a single group whose choruses were highly distinct). These results suggest that group choruses play an important role in intra-group signaling, potentially in contexts such as group formation, reinforcement of social bonds within the group, and/or collective decision-making, and they motivate new research questions about the role of collective signaling in social evolution.     

Bacterial linguistic communication and social intelligence

Bacteria have developed intricate communication capabilities (e.g. quorum-sensing, chemotactic signaling and plasmid exchange) to cooperatively self-organize into highly structured colonies with elevated environmental adaptability. We propose that bacteria use their intracellular flexibility, involving signal transduction networks and genomic plasticity, to collectively maintain linguistic communication: self and shared interpretations of chemical cues, exchange of chemical messages (semantic) and dialogues (pragmatic). Meaning-based communication permits colonial identity, intentional behavior (e.g. pheromone-based courtship for mating), purposeful alteration of colony structure (e.g. formation of fruiting bodies), decision-making (e.g. to sporulate) and the recognition and identification of other colonies - features we might begin to associate with a bacterial social intelligence. Such a social intelligence, should it exist, would require going beyond communication to encompass unknown additional intracellular processes to generate inheritable colonial memory and commonly shared genomic context.     

Quorum sensing and communication in bacteria

Bacteria are able “to sense” an increase in the cell population density and to respond to it by the induction of special sets of genes. This type of regulation, called Quorum Sensing (QS), includes the production and excretion of low-molecular-weight signaling molecules (autoinducers, AI), which diffuse readily through the cell wall, from cells into the medium. As the bacterial population reaches the critical level of density, the concentration of these signaling molecules in the medium increases as a function of population density. On reaching the critical threshold concentration, AIs bind to specific receptor regulatory proteins, which induce the expression of target genes. By means of AIs, bacteria accomplish the communication that is the transmission of information between bacteria belonging to the same or different species, genera, and even families: the signaling molecules of some bacteria affect the receptors of others causing a coordinated reply of cells of the bacterial population. Bacteria of different taxonomic groups use the QS systems in regulation of a broad range of physiological activities. These processes include virulence, symbiosis, conjugation, biofilm formation, bioluminescence, synthesis of enzymes, antibiotic substances, etc. Here we review different QS systems of bacteria, the role of QS in bacterial communication, and some applied aspects of QS regulation application.     

Social Calls Provide Tree‐dwelling Bats with Information about the Location of Conspecifics at Roosts

Animals can use signals emitted by other animals as sources of information. Auditory signals are important in communication networks, as they can potentially convey information about the location and state of conspecifics and other species over long distances. Signalling is important in fission–fusion societies, in which animals from the same social group temporarily split into subgroups and frequently change roost sites. We used playbacks of social calls of the noctule Nyctalus noctula produced in roosts, to show how bats might maintain group cohesion and to test the hypothesis that noctules can locate conspecifics when returning from foraging trips by eavesdropping on or communicating with roosting individuals. Noctules responded strongly to broadcasted social calls. Their reactions included inspections and landing on a loudspeaker broadcasting social calls and occasional social vocalisation. Responses by other bat species to the noctule social calls were negligible. The high amplitude, low‐frequency vocalisations emitted by noctules in roosts can propagate over long distances and allow group members to announce their position. Bats can extract information about the location of roosts containing conspecifics by eavesdropping or by communication. Social calls may thus be sufficient to locate conspecifics in roosts and maintain spatial associations of groups in mammals.     

Secreted bacterial phospholipase A2 enzymes: better living through phospholipolysis

Phospholipases are ubiquitous and diverse enzymes that induce changes in membrane composition, activate the inflammatory cascade and alter cell signaling pathways. Recent evidence suggests that certain bacterial pathogens have acquired genes encoding secreted phospholipase A2 enzymes through lateral gene transfer events. The two best-studied members of this class of enzyme are ExoU and SlaA, which are produced by Pseudomonas aeruginosa and group A Streptococcus, respectively. These enzymes modulate the host inflammatory response, increase the severity of disease and otherwise alter host-pathogen interactions. We propose that a key function of ExoU and SlaA is to increase the fitness of the subclones expressing these enzymes, thereby increasing the population size of the PLA2-positive strains and enhancing the likelihood of encountering an at-risk host.     

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.     

Social complexity as a proximate and ultimate factor in communicative complexity

The 'social complexity hypothesis' for communication posits that groups with complex social systems require more complex communicative systems to regulate interactions and relations among group members. Complex social systems, compared with simple social systems, are those in which individuals frequently interact in many different contexts with many different individuals, and often repeatedly interact with many of the same individuals in networks over time. Complex communicative systems, compared with simple communicative systems, are those that contain a large number of structurally and functionally distinct elements or possess a high amount of bits of information. Here, we describe some of the historical arguments that led to the social complexity hypothesis, and review evidence in support of the hypothesis. We discuss social complexity as a driver of communication and possible causal factor in human language origins. Finally, we discuss some of the key current limitations to the social complexity hypothesis-the lack of tests against alternative hypotheses for communicative complexity and evidence corroborating the hypothesis from modalities other than the vocal signalling channel.     

The study of vocal communication of wild mandrills in Cameroon in relation to their social structure

The vocal repertoire of the mandrill (Mandrillus sphinx), a forest living baboon, is described, and their vocal communication analyzed quantitatively. Although the vocal repertoire of mandrills corresponds well to that of savanna living baboons,Papio, some characteristics differed, such as the development of long-distance calls and differentiation of vocalizations between age-sex classes. Vocal communication within a group was closely related to changes in the spatial distribution of group members, and the two most common vocalizations, crowing and 2PG, appear to function as contact calls. Based on the wide dispersion of food trees, a group of mandrills divided into several feeding groups (subgroups). The two types of contact call were given in different and in some senses complementary contexts, and helped to facilitate and maintain group integration. According to their acoustic structure, these calls are long distance calls. Influenced by the high-level of attenuation of vocalization on the forest floor, the mandrill has developed them as contact calls, instead of using the contact “grunt,” which is common to the savanna living baboons. Comparing the patterns of vocal exchanges of mandrills with those of gelada and hamadryas baboons which have a multi-levelled society, the social structure of the mandrill is discussed. From the analysis of the spatial distribution of vocal emission, a number of clusters of vocalizations were obtained. These clusters correspond to subgroups. The frequent female-female and female-male vocal exchange between subgroups of mandrills suggest that the relationships between subgroups are less closed than between the one-male units of gelada and hamadryas baboons. Furthermore some of these clusters include more than two vocalizing adult males, while in other clusters there are no vocalizing adult males. Thus, the social structure of mandrills is suggested to be multi-male rather than a multilevelled type. The absence of contact calls specific for short distance and the functional replacement of the grunting of all group members by persistent emission of a loud call (2PG) by usually just one adult male suggests that the social structure of mandrills is not exactly equivalent to that of the multimale troop of savanna living baboons. Usually the use of 2PG is monopolized by one adult male travelling in the rear part of the group. Such monopolization of 2PG emission and the pattern of 2PG-2PG or 2PG-roar exchanges by adult males in some cases indicate the existence of strong dominance relationships among adult males, and especially the existence of a leader male within a multi-male group of mandrills.     

细菌的光响应及其机制研究进展

光作为一种环境信号,对细菌的生长和代谢有广泛的调节作用。对于光合细菌来讲,一方面,感光蛋白可以协助光合细菌游向最适的光环境,以利于其细胞内的光系统进行光合作用;另一方面,一些光合细菌可以感受并捕获光能为代谢提供能量。目前发现有些非光合细菌也有光响应,感光蛋白在细菌基因组内是普遍存在的,而且与细菌的一些生理功能有关。本文以非光合细菌为主介绍了目前在细菌中发现的趋光现象及其响应机制。     

Communicative roots of complex sociality and cognition

Mammals living in more complex social groups typically have large brains for their body size and many researchers have proposed that the primary driver of the increase in brain size through primate and hominin evolution was the selection pressures associated with sociality. Many mammals, and especially primates, use flexible signals that show a high degree of voluntary control and these signals may play an important role in forming and maintaining social relationships between group members. However, the specific role that cognitive skills play in this complex communication, and how in turn this relates to sociality, is still unclear. The hypothesis for the communicative roots of complex sociality and cognition posits that cognitive demands behind the communication needed to form and maintain bonded social relationships in complex social settings drives the link between brain size and sociality. We review the evidence in support of this hypothesis and why key features of cognitively complex communication such as intentionality and referentiality should be more effective in forming and maintaining bonded relationships as compared with less cognitively complex communication. Exploring the link between cognition, communication and sociality provides insights into how increasing flexibility in communication can facilitate the emergence of social systems characterised by bonded social relationships, such as those found in non‐human primates and humans. To move the field forward and carry out both within‐ and among‐species comparisons, we advocate the use of social network analysis, which provides a novel way to describe and compare social structure. Using this approach can lead to a new, systematic way of examining social and communicative complexity across species, something that is lacking in current comparative studies of social structure.     

Population Model of Quorum Sensing with Multiple Parallel Pathways

Quorum sensing (QS) is a bacterial communication mechanism that uses signal-receptor binding to regulate gene expression based on cell density, resulting in group behaviors such as biofilm formation, bioluminescence and stress response. In certain bacterial species such as Vibrio harveyi, several parallel QS signaling pathways drive a single phosphorylation–dephosphorylation cycle, which in turn regulates QS target genes. In this paper, we investigate the possible role of parallel signaling pathways by developing a mathematical model of QS in V. harveyi at both the single-cell and population levels. First we explore how signal integration may be achieved at the single-cell level, and how different model parameters influence the process. We then consider two examples of signal integration at the population level: a one-population model responding to two environmental cues (cell density and mass transfer), and a two-population model with distinct cell densities. In each case, we use contraction analysis to reduce the population model to an effective single-cell model.     

An S-locus receptor-like kinase plays a role as a negative regulator in plant defense responses

Plant cells often use cell surface receptors to sense environmental changes and then transduce external signals via activated signaling pathways to trigger adaptive responses. In Arabidopsis, the receptor-like protein kinase (RLK) gene family contains more than 600 members, and some of these are induced by pathogen infection, suggesting a possible role in plant defense responses. We previously characterized an S-locus RLK (CBRLK1) at the biochemical level. In this study, we examined the physiological function of CBRLK1 in defense responses. CBRLK1 mutant and CBRLK1-overexpressing transgenic plants showed enhanced and reduced resistance against a virulent bacterial pathogen, respectively. The altered pathogen resistances of the mutant and overexpressing transgenic plants were associated with increased and reduced induction of the pathogenesis-related gene PR1, respectively. These results suggest that CBRLK1 plays a negative role in the disease resistance signaling pathway in Arabidopsis.     

Costly signaling and cooperation.

We propose an explanation of cooperation among unrelated members of a social group in which cooperation evolves because it constitutes an honest signal of the member's quality as a mate, coalition partner or competitor, and therefore results in advantageous alliances for those signaling in this manner. Our model is framed as a multi-player public goods game that involves no repeated or assortative interactions, so that non-cooperation would be a dominant strategy if there were no signaling benefits. We show that honest signaling of underlying quality by providing a public good to group members can be evolutionarily stable, and can proliferate in a population in which it is initially rare, provided that certain plausible conditions hold, including a link between group-beneficial signaling and underlying qualities of the signaler that would be of benefit to a potential mate or alliance partner. Our model applies to a range of cooperative interactions, including unconditionally sharing individually consumable resources, participating in group raiding or defense, and punishing free-riding or other violations of social norms.     

Genomic features of lactic acid bacteria effecting bioprocessing and health

The lactic acid bacteria are a functionally related group of organisms known primarily for their bioprocessing roles in food and beverages. More recently, selected members of the lactic acid bacteria have been implicated in a number of probiotic roles that impact general health and well-being. Genomic analyses of multiple members of the lactic acid bacteria, at the genus, species, and strain level, have now elucidated many genetic features that direct their fermentative and probiotic roles. This information is providing an important platform for understanding core mechanisms that control and regulate bacterial growth, survival, signaling, and fermentative processes and, in some cases, potentially underlying probiotic activities within complex microbial and host ecosystems.     

LuxS quorum sensing: more than just a numbers game

Quorum sensing is a process of bacterial cell-to-cell communication involving the production and detection of extracellular signaling molecules called autoinducers. Quorum sensing allows populations of bacteria to collectively control gene expression, and thus synchronize group behavior. Processes controlled by quorum sensing are typically ones that are unproductive unless many bacteria act together. Most autoinducers enable intraspecies communication; however, a recently discovered autoinducer AI-2 has been proposed to serve as a 'universal signal' for interspecies communication. Studies suggest that AI-2 encodes information in addition to specifics about cell number.