S. Brook Peterson

Bacterial competition: surviving and thriving in the microbial jungle

Most natural environments harbour a stunningly diverse collection of microbial species. In these communities, bacteria compete with their neighbours for space and resources. Laboratory experiments with pure and mixed cultures have revealed many active mechanisms by which bacteria can impair or kill other microorganisms. In addition, a growing body of theoretical and experimental population studies indicates that the interactions within and between bacterial species can have a profound impact on the outcome of competition in nature. The next challenge is to integrate the findings of these laboratory and theoretical studies and to evaluate the predictions that they generate in more natural settings.

Type VI secretion system effectors: poisons with a purpose

The type VI secretion system (T6SS) mediates interactions between a broad range of Gram-negative bacterial species. Recent studies have led to a substantial increase in the number of characterized T6SS effector proteins and a more complete and nuanced view of the adaptive importance of the system. Although the T6SS is most often implicated in antagonism, in this Review, we consider the case for its involvement in both antagonistic and non-antagonistic behaviours. Clarifying the roles that type VI secretion has in microbial communities will contribute to broader efforts to understand the importance of microbial interactions in maintaining human and environmental health, and will inform efforts to manipulate these interactions for therapeutic or environmental benefit.

Rules of Engagement: Interspecies Interactions that Regulate Microbial Communities

Microbial communities comprise an interwoven matrix of biological diversity modified by physical and chemical variation over space and time. Although these communities are the major drivers of biosphere processes, relatively little is known about their structure and function, and predictive modeling is limited by a dearth of comprehensive ecological principles that describe microbial community processes. Here we discuss working definitions of central ecological terms that have been used in various fashions in microbial ecology, provide a framework by focusing on different types of interactions within communities, review the status of the interface between evolutionary and ecological study, and highlight important similarities and differences between macro- and microbial ecology. We describe current approaches to study microbial ecology and progress toward predictive modeling.

A Type VI Secretion-Related Pathway in Bacteroidetes Mediates Interbacterial Antagonism

Bacteroidetes are a phylum of Gram-negative bacteria abundant in mammalian-associated polymicrobial communities, where they impact digestion, immunity, and resistance to infection. Despite the extensive competition at high cell density that occurs in these settings, cell contact-dependent mechanisms of interbacterial antagonism, such as the type VI secretion system (T6SS), have not been defined in this group of organisms. Herein we report the bioinformatic and functional characterization of a T6SS-like pathway in diverse Bacteroidetes. Using prominent human gut commensal and soil-associated species, we demonstrate that these systems localize dynamically within the cell, export antibacterial proteins, and target competitor bacteria. The Bacteroidetes system is a distinct pathway with marked differences in gene content and high evolutionary divergence from the canonical T6S pathway. Our findings offer a potential molecular explanation for the abundance of Bacteroidetes in polymicrobial environments, the observed stability of Bacteroidetes in healthy humans, and the barrier presented by the microbiota against pathogens.

Breaching the great wall: peptidoglycan and microbial interactions

Once thought to be a process that occurred only in a few human pathogens, release of biologically active peptidoglycan fragments during growth by Gram-negative bacteria controls many types of bacterial interaction, including symbioses and interactions between microorganisms. This Perspective explores the role of peptidoglycan fragments in mediating a range of microbial?host interactions, and discusses the many systems in which peptidoglycan fragments released during bacterial growth might be active.

Environmental distribution and population biology of Candidatus Accumulibacter, a primary agent of biological phosphorus removal

Members of the uncultured bacterial genus Candidatus Accumulibacter are capable of intracellular accumulation of inorganic phosphate in activated sludge wastewater treatment plants (WWTPs) performing enhanced biological phosphorus removal, but were also recently shown to inhabit freshwater and estuarine sediments. Additionally, metagenomic sequencing of two bioreactor cultures enriched in Candidatus Accumulibacter, but housed on separate continents, revealed the potential for global dispersal of particular Candidatus Accumulibacter strains, which we hypothesize is facilitated by the ability of Candidatus Accumulibacter to persist in environmental habitats. In the current study, we used sequencing of a phylogenetic marker, the ppk1 gene, to characterize Candidatus Accumulibacter populations in diverse environments, at varying distances from WWTPs. We discovered several new lineages of Candidatus Accumulibacter which had not previously been detected in WWTPs, and also uncovered new diversity and structure within previously detected lineages. Habitat characteristics were found to be a key determinant of Candidatus Accumulibacter lineage distribution while, as predicted, geographic distance played little role in limiting dispersal on a regional scale. However, on a local scale, enrichment of particular Candidatus Accumulibacter lineages in WWTP appeared to impact local environmental populations. These results provide evidence of ecological differences among Candidatus Accumulibacter lineages.

Kin cell lysis is a danger signal that activates antibacterial pathways of Pseudomonas aeruginosa

The perception and response to cellular death is an important aspect of multicellular eukaryotic life. For example, damage-associated molecular patterns activate an inflammatory cascade that leads to removal of cellular debris and promotion of healing. We demonstrate that lysis of Pseudomonas aeruginosa cells triggers a program in the remaining population that confers fitness in interspecies co-culture. We find that this program, termed P. aeruginosa response to antagonism (PARA), involves rapid deployment of antibacterial factors and is mediated by the Gac/Rsm global regulatory pathway. Type VI secretion, and, unexpectedly, conjugative type IV secretion within competing bacteria, induce P. aeruginosa lysis and activate PARA, thus providing a mechanism for the enhanced capacity of P. aeruginosa to target bacteria that elaborate these factors. Our finding that bacteria sense damaged kin and respond via a widely distributed pathway to mount a complex response raises the possibility that danger sensing is an evolutionarily conserved process. DOI: http://dx.doi.org/10.7554/eLife.05701.001

Transferred interbacterial antagonism genes augment eukaryotic innate immune function

Horizontal gene transfer allows organisms to rapidly acquire adaptive traits. Although documented instances of horizontal gene transfer from bacteria to eukaryotes remain rare, bacteria represent a rich source of new functions potentially available for co-option. One benefit that genes of bacterial origin could provide to eukaryotes is the capacity to produce antibacterials, which have evolved in prokaryotes as the result of eons of interbacterial competition. The type VI secretion amidase effector (Tae) proteins are potent bacteriocidal enzymes that degrade the cell wall when delivered into competing bacterial cells by the type VI secretion system. Here we show that tae genes have been transferred to eukaryotes on at least six occasions, and that the resulting domesticated amidase effector (dae) genes have been preserved for hundreds of millions of years through purifying selection. We show that the dae genes acquired eukaryotic secretion signals, are expressed within recipient organisms, and encode active antibacterial toxins that possess substrate specificity matching extant Tae proteins of the same lineage. Finally, we show that a dae gene in the deer tick Ixodes scapularis limits proliferation of Borrelia burgdorferi, the aetiologic agent of Lyme disease. Our work demonstrates that a family of horizontally acquired toxins honed to mediate interbacterial antagonism confers previously undescribed antibacterial capacity to eukaryotes. We speculate that the selective pressure imposed by competition between bacteria has produced a reservoir of genes encoding diverse antimicrobial functions that are tailored for co-option by eukaryotic innate immune systems.

Secreted Effectors Encoded within and outside of the Francisella Pathogenicity Island Promote Intramacrophage Growth

The intracellular bacterial pathogen Francisella tularensis causes tularemia, a zoonosis that can be fatal. The type VI secretion system (T6SS) encoded by the Francisella pathogenicity island (FPI) is critical for the virulence of this organism. Existing studies suggest that the complete repertoire of T6SS effectors delivered to host cells is encoded by the FPI. Using a proteome-wide approach, we discovered that the FPI-encoded T6SS exports at least three effectors encoded outside of the island. These proteins share features with virulence determinants of other pathogens, and we provide evidence that they can contribute to intramacrophage growth. The remaining proteins that we identified are encoded within the FPI. Two of these FPI-encoded proteins constitute effectors, whereas the others form a unique complex required for core function of the T6SS apparatus. The discovery of secreted effectors mediating interactions between Francisella and its host significantly advances our understanding of the pathogenesis of this organism.

A broadly distributed toxin family mediates contact-dependent antagonism between gram-positive bacteria

The Firmicutes are a phylum of bacteria that dominate numerous polymicrobial habitats of importance to human health and industry. Although these communities are often densely colonized, a broadly distributed contact-dependent mechanism of interbacterial antagonism utilized by Firmicutes has not been elucidated. Here we show that proteins belonging to the LXG polymorphic toxin family present in Streptococcus intermedius mediate cell contact- and Esx secretion pathway-dependent growth inhibition of diverse Firmicute species. The structure of one such toxin revealed a previously unobserved protein fold that we demonstrate directs the degradation of a uniquely bacterial molecule required for cell wall biosynthesis, lipid II. Consistent with our functional data linking LXG toxins to interbacterial interactions in S. intermedius, we show that LXG genes are prevalent in the human gut microbiome, a polymicrobial community dominated by Firmicutes. We speculate that interbacterial antagonism mediated by LXG toxins plays a critical role in shaping Firmicute-rich bacterial communities. DOI: http://dx.doi.org/10.7554/eLife.26938.001