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1. Diversification of Type VI Secretion System Toxins Reveals Ancient Antagonism among Bee Gut Microbes

   https://doi.org/10.1128/mBio.01630-17  

   Steele, Margaret I.; Kwong, Waldan K.; Whiteley, Marvin; Moran, Nancy A.; Lindow, Steven E. (December 2017, mBio)

   ABSTRACT Microbial communities are shaped by interactions among their constituent members. Some Gram-negative bacteria employ type VI secretion systems (T6SSs) to inject protein toxins into neighboring cells. These interactions have been theorized to affect the composition of host-associated microbiomes, but the role of T6SSs in the evolution of gut communities is not well understood. We report the discovery of two T6SSs and numerous T6SS-associated Rhs toxins within the gut bacteria of honey bees and bumble bees. We sequenced the genomes of 28 strains of Snodgrassella alvi , a characteristic bee gut microbe, and found tremendous variability in their Rhs toxin complements: altogether, these strains appear to encode hundreds of unique toxins. Some toxins are shared with Gilliamella apicola , a coresident gut symbiont, implicating horizontal gene transfer as a source of toxin diversity in the bee gut. We use data from a transposon mutagenesis screen to identify toxins with antibacterial function in the bee gut and validate the function and specificity of a subset of these toxin and immunity genes in Escherichia coli . Using transcriptome sequencing, we demonstrate that S. alvi T6SSs and associated toxins are upregulated in the gut environment. We find that S. alvi Rhs loci have a conserved architecture, consistent with the C-terminal displacement model of toxin diversification, with Rhs toxins, toxin fragments, and cognate immunity genes that are expressed and confer strong fitness effects in vivo . Our findings of T6SS activity and Rhs toxin diversity suggest that T6SS-mediated competition may be an important driver of coevolution within the bee gut microbiota. IMPORTANCE The structure and composition of host-associated bacterial communities are of broad interest, because these communities affect host health. Bees have a simple, conserved gut microbiota, which provides an opportunity to explore interactions between species that have coevolved within their host over millions of years. This study examined the role of type VI secretion systems (T6SSs)—protein complexes used to deliver toxic proteins into bacterial competitors—within the bee gut microbiota. We identified two T6SSs and diverse T6SS-associated toxins in bacterial strains from bees. Expression of these genes is increased in bacteria in the bee gut, and toxin and immunity genes demonstrate antibacterial and protective functions, respectively, when expressed in Escherichia coli . Our results suggest that coevolution among bacterial species in the bee gut has favored toxin diversification and maintenance of T6SS machinery, and demonstrate the importance of antagonistic interactions within host-associated microbial communities. 

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2. Intraspecific antagonism through viral toxin encoded by chronic Sulfolobus spindle-shaped virus

   https://doi.org/10.1098/rstb.2020.0476  

   DeWerff, Samantha J.; Zhang, Changyi; Schneider, John; Whitaker, Rachel J. (January 2022, Philosophical Transactions of the Royal Society B: Biological Sciences)

   Virus–host interactions evolve along a symbiosis continuum from antagonism to mutualism. Long-term associations between virus and host, such as those in chronic infection, will select for traits that drive the interaction towards mutualism, especially when susceptible hosts are rare in the population. Virus–host mutualism has been demonstrated in thermophilic archaeal populations where Sulfolobus spindle-shaped viruses (SSVs) provide a competitive advantage to their host Sulfolobus islandicus by producing a toxin that kills uninfected strains. Here, we determine the genetic basis of this killing phenotype by identifying highly transcribed genes in cells that are chronically infected with a diversity of SSVs. We demonstrate that these genes alone confer growth inhibition by being expressed in uninfected cells via a Sulfolobus expression plasmid. Challenge of chronically infected strains with vector-expressed toxins revealed a nested network of cross-toxicity among divergent SSVs, with both broad and specific toxin efficacies. This suggests that competition between viruses and/or their hosts could maintain toxin diversity. We propose that competitive interactions among chronic viruses to promote their host fitness form the basis of virus–host mutualism. This article is part of the theme issue ‘The secret lives of microbial mobile genetic elements’. 

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3. Higher-order effects, continuous species interactions, and trait evolution shape microbial spatial dynamics

   https://doi.org/10.1073/pnas.2020956119  

   Swain, Anshuman; Fussell, Levi; Fagan, William F. (January 2022, Proceedings of the National Academy of Sciences)

   The assembly and maintenance of microbial diversity in natural communities, despite the abundance of toxin-based antagonistic interactions, presents major challenges for biological understanding. A common framework for investigating such antagonistic interactions involves cyclic dominance games with pairwise interactions. The incorporation of higher-order interactions in such models permits increased levels of microbial diversity, especially in communities in which antibiotic-producing, sensitive, and resistant strains coexist. However, most such models involve a small number of discrete species, assume a notion of pure cyclic dominance, and focus on low mutation rate regimes, none of which well represent the highly interlinked, quickly evolving, and continuous nature of microbial phenotypic space. Here, we present an alternative vision of spatial dynamics for microbial communities based on antagonistic interactions—one in which a large number of species interact in continuous phenotypic space, are capable of rapid mutation, and engage in both direct and higher-order interactions mediated by production of and resistance to antibiotics. Focusing on toxin production, vulnerability, and inhibition among species, we observe highly divergent patterns of diversity and spatial community dynamics. We find that species interaction constraints (rather than mobility) best predict spatiotemporal disturbance regimes, whereas community formation time, mobility, and mutation size best explain patterns of diversity. We also report an intriguing relationship among community formation time, spatial disturbance regimes, and diversity dynamics. This relationship, which suggests that both higher-order interactions and rapid evolution are critical for the origin and maintenance of microbial diversity, has broad-ranging links to the maintenance of diversity in other systems. 

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4. Selection for toxin production in spatially structured environments increases with growth rate

   https://doi.org/10.1093/ismejo/wraf061  

   Bisesi, Ave T; Chacón, Jeremy M; Smanski, Michael J; Kinkel, Linda; Harcombe, William R (April 2025, The ISME Journal)

   Abstract Microbes adopt a diversity of strategies to successfully compete with coexisting strains for space and resources. One common strategy is the production of toxic compounds to inhibit competitors, but the strength and direction of selection for this strategy varies depending on the environment. Existing theoretical and experimental evidence suggests growth in spatially structured environments makes toxin production more beneficial because competitive interactions are localized. Because higher growth rates reduce the length-scale of interactions in structured environments, theory predicts that toxin production should be especially beneficial under these conditions. We tested this hypothesis by developing a genome-scale metabolic modeling approach and complementing it with comparative genomics to investigate the impact of growth rate on selection for costly toxin production. Our modeling approach expands the current abilities of the dynamic flux balance analysis platform COMETS to incorporate signaling and toxin production. Using this capability, we find that our modeling framework predicts that the strength of selection for toxin production increases as growth rate increases. This finding is supported by comparative genomics analyses that include diverse microbial species. Our work emphasizes that toxin production is more likely to be maintained in rapidly growing, spatially structured communities, thus improving our ability to manage microbial communities and informing natural product discovery. 

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5. The temporal and spatial dimensions of plant–soil feedbacks

   https://doi.org/10.1111/nph.18719  

   Chung, Y. Anny (February 2023, New Phytologist)

   Summary Feedbacks between plants and soil microbes form a keystone to terrestrial community and ecosystem dynamics. Recent advances in dissecting the spatial and temporal dynamics of plant–soil feedbacks (PSFs) have challenged longstanding assumptions of spatially well‐mixed microbial communities and exceedingly fast microbial assembly dynamics relative to plant lifespans. Instead, PSFs emerge from interactions that are inherently mismatched in spatial and temporal scales, and explicitly considering these spatial and temporal dynamics is crucial to understanding the contribution of PSFs to foundational ecological patterns. I propose a synthetic spatiotemporal framework for future research that pairs experimental and modeling approaches grounded in mechanism to improve predictability and generalizability of PSFs. 

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