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1. Phage-Encoded Sigma Factors Alter Bacterial Dormancy

   https://doi.org/10.1128/msphere.00297-22  

   Schwartz, D. A. ; Lehmkuhl, B. K. ; Lennon, J. T. ( August 2022 , mSphere)

   Imperiale, Michael J. (Ed.)

   ABSTRACT By entering a reversible state of reduced metabolic activity, dormant microorganisms are able to tolerate suboptimal conditions that would otherwise reduce their fitness. Dormancy may also benefit bacteria by serving as a refuge from parasitic infections. Here, we focus on dormancy in the Bacillota , where endospore development is transcriptionally regulated by the expression of sigma factors. A disruption of this process could influence the survivorship or reproduction of phages that infect spore-forming hosts with implications for coevolutionary dynamics. We characterized the distribution of sigma factors in over 4,000 genomes of diverse phages capable of infecting hosts that span the bacterial domain. From this, we identified homologs of sporulation-specific sigma factors in phages that infect spore-forming hosts. Unlike sigma factors required for phage reproduction, we provide evidence that sporulation-like sigma factors are nonessential for lytic infection. However, when expressed in the spore-forming Bacillus subtilis , some of these phage-derived sigma factors can activate the bacterial sporulation gene network and lead to a reduction in spore yield. Our findings suggest that the acquisition of host-like transcriptional regulators may allow phages to manipulate a complex and ancient trait in one of the most abundant cell types on Earth. IMPORTANCE As obligate parasites, phages exert strong top-down pressure on host populations with eco-evolutionary implications for community dynamics and ecosystem functioning. The process of phage infection, however, is constrained by bottom-up processes that influence the energetic and nutritional status of susceptible hosts. Many phages have acquired auxiliary genes from bacteria, which can be used to exploit host metabolism with consequences for phage fitness. In this study, we demonstrate that phages infecting spore-forming bacteria carry homologs of sigma factors, which their hosts use to orchestrate gene expression during spore development. By tapping into regulatory gene networks, phages may manipulate the physiology and survival strategies of nongrowing bacteria in ways that influence host-parasite coevolution. 

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2. Resuscitation of the microbial seed bank alters plant‐soil interactions

   https://doi.org/10.1111/mec.15932  

   Kuo, Venus ; Lehmkuhl, Brent K. ; Lennon, Jay T. ( May 2021 , Molecular Ecology)

   While microorganisms are recognized for driving belowground processes that influence the productivity and fitness of plant populations, the vast majority of bacteria and fungi in soil belong to a seed bank consisting of dormant individuals. However, plant performance may be affected by microbial dormancy through its effects on the activity, abundance, and diversity of soil microorganisms. To test how microbial seed banks influence plant‐soil interactions, we purified recombinant resuscitation promoting factor (Rpf), a bacterial protein that terminates dormancy. In a factorially designed experiment, we then applied the Rpf to soil containing field mustard (Brassicarapa), an agronomically important plant species. Plant biomass was ~33% lower in the Rpf treatment compared to plants grown with an unmanipulated microbial seed bank. In addition, Rpf reduced soil respiration, decreased bacterial abundance, and increased fungal abundance. These effects of Rpf on plant performance were accompanied by shifts in bacterial community composition, which may have diluted mutualists or resuscitated pathogens. Our findings suggest that changes in microbial seed banks may influence the magnitude and direction of plant‐soil feedbacks in ways that affect above‐ and belowground biodiversity and function.

    

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3. Phage-encoded sigma factors alter bacterial dormancy

   https://doi.org/10.1101/2021.11.12.468384  

   Schwartz DA, Lekmkuhl BK ( January 2021 , bioRxiv)

   By entering a reversible state of reduced metabolic activity, dormant microorganisms are able to tolerate suboptimal conditions that would otherwise reduce their fitness. Dormancy may also benefit bacteria by serving as a refuge from parasitic infections. Here we focus on dormancy in the Firmicutes, where endospore development is transcriptionally regulated by the expression of sigma factors. A disruption of this process could influence the survivorship and reproduction of phages that infect spore-forming hosts with implications for coevolutionary dynamics. Here, we characterized the distribution and diversity of sigma factors in nearly 3,500 phage genomes. Homologs of sporulation-specific sigma factors were identified in phages that infect spore-forming hosts. Unlike sigma factors required for phage reproduction, the sporulation-like sigma factors were non-essential for lytic infection. However, when expressed in the spore-forming Bacillus subtilis, sigma factors from phages activated the bacterial sporulation gene network and reduced spore yield. Our findings suggest that the acquisition of host-like transcriptional regulators may allow phages to manipulate a complex and ancient trait in one of the most abundant cell types on Earth. 

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4. Stabilising role of seed banks and the maintenance of bacterial diversity

   https://doi.org/10.1111/ele.13853  

   Wisnoski, Nathan I. ; Lennon, Jay T. ; Reynolds, ed., Heather ( July 2021 , Ecology Letters)

   Coexisting species often exhibit negative frequency dependence due to mechanisms that promote population growth and persistence when rare. These stabilising mechanisms can maintain diversity through interspecific niche differences, but also through life‐history strategies like dormancy that buffer populations in fluctuating environments. However, there are few tests demonstrating how seed banks contribute to long‐term community dynamics and the maintenance of diversity. Using a multi‐year, high‐frequency time series of bacterial community data from a north temperate lake, we documented patterns consistent with stabilising coexistence. Bacterial taxa exhibited differential responses to seasonal environmental conditions, while seed bank dynamics helped maintain diversity over less‐favourable winter periods. Strong negative frequency dependence in rare, but metabolically active, taxa suggested a role for biotic interactions in promoting coexistence. Together, our results provide field‐based evidence that niche differences and seed banks contribute to recurring community dynamics and the long‐term maintenance of diversity in nature.

    

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5. Bacterial resistance response and resource availability mediate viral coexistence

   https://doi.org/10.1093/jeb/voae022  

   Butt, Lisa ; Meyer, Justin R. ; Lindsay, Richard J. ; Beardmore, Robert E. ; Gudelj, Ivana ( February 2024 , Journal of Evolutionary Biology)

   Viruses that infect bacteria, known as bacteriophages or phages, are the most prevalent entities on Earth. Their genetic diversity in nature is well documented, and members of divergent lineages can be found sharing the same ecological niche. This viral diversity can be influenced by a number of factors, including productivity, spatial structuring of the environment, and host-range trade-offs. Rapid evolution is also known to promote diversity by buffering ecological systems from extinction. There is, however, little known about the impact of coevolution on the maintenance of viral diversity within a microbial community. To address this, we developed a 4 species experimental system where two bacterial hosts, a generalist and a specialist phage, coevolved in a spatially homogenous environment over time. We observed the persistence of both viruses if the resource availability was sufficiently high. This coexistence occurred in the absence of any detectable host-range trade-offs that are costly for generalists and thus known to promote viral diversity. However, the coexistence was lost if two bacteria were not permitted to evolve alongside the phages or if two phages coevolved with a single bacterial host. Our findings indicate that a host’s resistance response in mixed-species communities plays a significant role in maintaining viral diversity in the environment.

    

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