Polybacterial human disease: the ills of social networking

Short, Francesca L.; Murdoch, Sarah; Ryan, Robert P.

doi:10.1016/j.tim.2014.05.007

Cited by 128 publications

(130 citation statements)

References 88 publications

(84 reference statements)

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“…It is a fundamental question if microbes in polymicrobial infections predominantly cooperate or compete with each other (4). To systematically identify such interaction patterns between pairs of isolates, we compared the occurrence of two-node subnetworks in the measured interaction network to that in an ensemble of randomized networks that preserve the degree distribution (SI Appendix, SI Methods).…”

Section: Significancementioning

confidence: 99%

See 1 more Smart Citation

Interaction networks, ecological stability, and collective antibiotic tolerance in polymicrobial infections

Vos

Zagórski

McNally

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

165

207

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Polymicrobial infections constitute small ecosystems that accommodate several bacterial species. Commonly, these bacteria are investigated in isolation. However, it is unknown to what extent the isolates interact and whether their interactions alter bacterial growth and ecosystem resilience in the presence and absence of antibiotics. We quantified the complete ecological interaction network for 72 bacterial isolates collected from 23 individuals diagnosed with polymicrobial urinary tract infections and found that most interactions cluster based on evolutionary relatedness. Statistical network analysis revealed that competitive and cooperative reciprocal interactions are enriched in the global network, while cooperative interactions are depleted in the individual host community networks. A population dynamics model parameterized by our measurements suggests that interactions restrict community stability, explaining the observed species diversity of these communities. We further show that the clinical isolates frequently protect each other from clinically relevant antibiotics. Together, these results highlight that ecological interactions are crucial for the growth and survival of bacteria in polymicrobial infection communities and affect their assembly and resilience. microbiology | systems biology | antibiotics | infection

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Section: Significancementioning

confidence: 99%

“…Interactions between microbes can alter the severity of infections (1,2) and complicate treatments (3)(4)(5)(6). Still, the interplay between microbes in clinical environments remains poorly understood, as clinical isolates are commonly investigated in isolation.…”

mentioning

confidence: 99%

Interaction networks, ecological stability, and collective antibiotic tolerance in polymicrobial infections

Vos

Zagórski

McNally

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

165

207

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“…They can range from fierce competition for nutrients and niches, manifested by antagonistic behavior, to highly evolved cooperative mechanisms between different species that support their mutual growth in specific environments. While other published articles have provided a detailed review of the studies that have been undertaken in an attempt to understand the mechanisms involved in these complex interactions [1,7,[9][10][11][13][14][15], our intent here is to provide the reader with information about the models that have been used to study polymicrobial interactions in biofilms. Thus, below we briefly define the major interactions that have been studied (Figure 1), and then discuss the models in which they have been examined in the following sections.…”

Section: Polymicrobial Interactions In Biofilmsmentioning

confidence: 99%

“…Microbial synergy can be defined as a cooperative interaction between two or more species of microbes that produces an effect not achieved by an individual species alone [1,7,[9][10][11][12][13][14]16] (Figure 1). In biofilms and biofilm-related infections, these 'effects' include increased growth, antimicrobial tolerance, virulence and persistence, and enhanced production of exopolysaccharide (EPS) [17][18][19][20][21][22][23][24][25][26][27][28].…”

Section: • Synergismmentioning

confidence: 99%

Biofilm Models of Polymicrobial Infection

2015

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Interactions between microbes are complex and play an important role in the pathogenesis of infections. These interactions can range from fierce competition for nutrients and niches to highly evolved cooperative mechanisms between different species that support their mutual growth. An increasing appreciation for these interactions, and desire to uncover the mechanisms that govern them, has resulted in a shift from monomicrobial to polymicrobial biofilm studies in different disease models. Here we provide an overview of biofilm models used to study select polymicrobial infections and highlight the impact that the interactions between microbes within these biofilms have on disease progression. Notable recent advances in the development of polymicrobial biofilm-associated infection models and challenges facing the study of polymicrobial biofilms are addressed. Polymicrobial interactions in biofilmsOver the past 2 decades there has been a revolutionary paradigm shift in the field of microbiology with the appreciation that bacteria present in most biological systems exist in biofilms, rather than in a free-living state. This understanding has dramatically changed the way we study bacteria in the laboratory and resulted in the development of many new experimental systems that replicate biofilm environments [1][2][3][4][5]. Studies utilizing these systems have demonstrated time and time again that bacteria behave very differently when in a biofilm than during planktonic growth. In many ways, we now have to relearn everything we thought we knew about bacterial behavior through the view of the biofilm lens.Similarly, the recent explosion of metagenomic studies has significantly increased our appreciation of the complexity of the microbial populations present in biofilms [6,7]. This is also true for infections, most of which are thought to be biofilm related and inherently polymicrobial, including various species of bacteria, fungi and viruses [8]. It is thought that microbes act in concert to establish biofilms, which in turn can increase tolerance to antimicrobials, exacerbate of the host's immune response and increase persistence at the infection site [7,[9][10][11].Genetic diversity of microbes within biofilm communities is thought to increase the fitness of the residing community, making them more equipped to survive environmental stresses. In large part, this is due to an expanded gene pool, which can be more easily shared within the confines of a biofilm community [12]. Community composition and interactions within the community can have huge influences on bacterial behavior. Thus, just as the behavior of planktonic versus biofilm-associated bacteria is dramatically different, so is that of bacteria in single species versus multispecies systems.Interactions between microbes are complex and highly dependent on context. They can range from fierce competition for nutrients and niches, manifested by antagonistic behavior, to highly evolved cooperative mechanisms between different species that support their mutual grow...

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“…In recent years, the practical value of studying such complex communities has increased, as both the polymicrobial nature of many infections (2) and symbioses (3) and the general role of microbial ecosystems in metazoan health (4,5) have become more fully appreciated. In parallel, novel sequencing technologies have offered new tools for understanding microbial community structures and dynamics.…”

mentioning

confidence: 99%

Death Becomes Them: Bacterial Community Dynamics and Stilbene Antibiotic Production in Cadavers of Galleria mellonella Killed by Heterorhabditis and Photorhabdus spp

Wollenberg

Jagdish

Slough

et al. 2016

Appl Environ Microbiol

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Insect larvae killed by entomopathogenic nematodes are thought to contain bacterial communities dominated by a single bacterial genus, that of the nematode's bacterial symbiont. In this study, we used next-generation sequencing to profile bacterial community dynamics in greater wax moth (Galleria mellonella) larvae cadavers killed by Heterorhabditis nematodes and their Photorhabdus symbionts. We found that, although Photorhabdus strains did initially displace an Enterococcus-dominated community present in uninfected G. mellonella insect larvae, the cadaver community was not static. Twelve days postinfection, Photorhabdus shared the cadaver with Stenotrophomonas species. Consistent with this result, Stenotrophomonas strains isolated from infected cadavers were resistant to Photorhabdus-mediated toxicity in solid coculture assays. We isolated and characterized a Photorhabdus-produced antibiotic from G. mellonella cadavers, produced it synthetically, and demonstrated that both the natural and synthetic compounds decreased G. mellonella-associated Enterococcus growth, but not Stenotrophomonas growth, in vitro. Finally, we showed that the Stenotrophomonas strains described here negatively affected Photorhabdus growth in vitro. Our results add an important dimension to a broader understanding of Heterorhabditis-Photorhabdus biology and also demonstrate that interspecific bacterial competition likely characterizes even a theoretically monoxenic environment, such as a Heterorhabditis-Photorhabdus-parasitized insect cadaver. IMPORTANCEUnderstanding, and eventually manipulating, both human and environmental health depends on a complete accounting of the forces that act on and shape microbial communities. One of these underlying forces is hypothesized to be resource competition. A resource that has received little attention in the general microbiological literature, but likely has ecological and evolutionary importance, is dead/decaying multicellular organisms. Metazoan cadavers, including those of insects, are ephemeral and nutrient-rich environments, where resource competition might shape interspecific macrobiotic and microbiotic interactions. This study is the first to use a next-generation sequencing approach to study the community dynamics of bacteria within a model insect cadaver system: insect larvae parasitized by entomopathogenic nematodes and their bacterial symbionts. By integrating bioinformatic, biochemical, and classic in vitro microbiological approaches, we have provided mechanistic insight into how antibiotic-mediated bacterial interactions may shape community dynamics within insect cadavers.

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Polybacterial human disease: the ills of social networking

Cited by 128 publications

References 88 publications

Interaction networks, ecological stability, and collective antibiotic tolerance in polymicrobial infections

Interaction networks, ecological stability, and collective antibiotic tolerance in polymicrobial infections

Biofilm Models of Polymicrobial Infection

Death Becomes Them: Bacterial Community Dynamics and Stilbene Antibiotic Production in Cadavers of Galleria mellonella Killed by Heterorhabditis and Photorhabdus spp

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