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1. Plasmid-Mediated Stabilization of Prophages

   https://doi.org/10.1128/msphere.00930-21  

   Tuttle, Matthew J.; May, Frank S.; Basso, Jonelle T.; Gann, Eric R.; Xu, Julie; Buchan, Alison (April 2022, mSphere)

   McMahon, Katherine (Ed.)

   ABSTRACT Mobile genetic elements (MGEs) drive bacterial evolution, alter gene availability within microbial communities, and facilitate adaptation to ecological niches. In natural systems, bacteria simultaneously possess or encounter multiple MGEs, yet their combined influences on microbial communities are poorly understood. Here, we investigate interactions among MGEs in the marine bacterium Sulfitobacter pontiacus . Two related strains, CB-D and CB-A, each harbor a single prophage. These prophages share high sequence identity with one another and an integration site within the host genome, yet these strains exhibit differences in “spontaneous” prophage induction (SPI) and consequent fitness. To better understand mechanisms underlying variation in SPI between these lysogens, we closed their genomes, which revealed that in addition to harboring different prophage genotypes, CB-A lacks two of the four large, low-copy-number plasmids possessed by CB-D. To assess the relative roles of plasmid content versus prophage genotype on host physiology, a panel of derivative strains varying in MGE content were generated. Characterization of these derivatives revealed a robust link between plasmid content and SPI, regardless of prophage genotype. Strains possessing all four plasmids had undetectable phage in cell-free lysates, while strains lacking either one plasmid (pSpoCB-1) or a combination of two plasmids (pSpoCB-2 and pSpoCB-4) produced high (>10 5 PFU/mL) phage titers. Homologous plasmid sequences were identified in related bacteria, and plasmid and phage genes were found to be widespread in Tara Oceans metagenomic data sets. This suggests that plasmid-dependent stabilization of prophages may be commonplace throughout the oceans. IMPORTANCE The consequences of prophage induction on the physiology of microbial populations are varied and include enhanced biofilm formation, conferral of virulence, and increased opportunity for horizontal gene transfer. These traits lead to competitive advantages for lysogenized bacteria and influence bacterial lifestyles in a variety of niches. However, biological controls of “spontaneous” prophage induction, the initiation of phage replication and phage-mediated cell lysis without an overt stressor, are not well understood. In this study, we observed a novel interaction between plasmids and prophages in the marine bacterium Sulfitobacter pontiacus . We found that loss of one or more distinct plasmids—which we show carry genes ubiquitous in the world’s oceans—resulted in a marked increase in prophage induction within lysogenized strains. These results demonstrate cross talk between different mobile genetic elements and have implications for our understanding of the lysogenic-lytic switches of prophages found not only in marine environments, but throughout all ecosystems. 

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2. Spontaneously Produced Lysogenic Phages Are an Important Component of the Soybean Bradyrhizobium Mobilome

   https://doi.org/10.1128/mbio.00295-23  

   Joglekar, Prasanna; Ferrell, Barbra D.; Jarvis, Tessa; Haramoto, Kona; Place, Nicole; Dums, Jacob T.; Polson, Shawn W.; Wommack, K. Eric; Fuhrmann, Jeffry J. (April 2023, mBio)

   Buchan, Alison (Ed.)

   ABSTRACT The ability of Bradyrhizobium spp. to nodulate and fix atmospheric nitrogen in soybean root nodules is critical to meeting humanity’s nutritional needs. The intricacies of soybean bradyrhizobia-plant interactions have been studied extensively; however, bradyrhizobial ecology as influenced by phages has received somewhat less attention, even though these interactions may significantly impact soybean yield. In batch culture, four soybean bradyrhizobia strains, Bradyrhizobium japonicum S06B (S06B-Bj), B. japonicum S10J (S10J-Bj), Bradyrhizobium diazoefficiens USDA 122 (USDA 122-Bd), and Bradyrhizobium elkanii USDA 76 T (USDA 76-Be), spontaneously (without apparent exogenous chemical or physical induction) produced tailed phages throughout the growth cycle; for three strains, phage concentrations exceeded cell numbers by ~3-fold after 48 h of incubation. Phage terminase large-subunit protein phylogeny revealed possible differences in phage packaging and replication mechanisms. Bioinformatic analyses predicted multiple prophage regions within each soybean bradyrhizobia genome, preventing accurate identification of spontaneously produced prophage (SPP) genomes. A DNA sequencing and mapping approach accurately delineated the boundaries of four SPP genomes within three of the soybean bradyrhizobia chromosomes and suggested that the SPPs were capable of transduction. In addition to the phages, S06B-Bj and USDA 76-Be contained three to four times more insertion sequences (IS) and large, conjugable, broad host range plasmids, both of which are known drivers of horizontal gene transfer (HGT) in soybean bradyrhizobia. These factors indicate that SPP along with IS and plasmids participate in HGT, drive bradyrhizobia evolution, and play an outsized role in bradyrhizobia ecology. IMPORTANCE Previous studies have shown that IS and plasmids mediate HGT of symbiotic nodulation ( nod ) genes in soybean bradyrhizobia; however, these events require close cell-to-cell contact, which could be limited in soil environments. Bacteriophage-assisted gene transduction through spontaneously produced prophages provides a stable means of HGT not limited by the constraints of proximal cell-to-cell contact. These phage-mediated HGT events may shape soybean bradyrhizobia population ecology, with concomitant impacts on soybean agriculture. 

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3. Natural and synthetic inhibitors of a phage-encoded quorum-sensing receptor affect phage–host dynamics in mixed bacterial communities

   https://doi.org/10.1073/pnas.2217813119  

   Silpe, Justin E.; Duddy, Olivia P.; Bassler, Bonnie L. (December 2022, Proceedings of the National Academy of Sciences)

   Viruses that infect bacteria, called phages, shape the composition of bacterial communities and are important drivers of bacterial evolution. We recently showed that temperate phages, when residing in bacteria (i.e., prophages), are capable of manipulating the bacterial cell-to-cell communication process called quorum sensing (QS). QS relies on the production, release, and population-wide detection of signaling molecules called autoinducers (AI). Gram-negative bacteria commonly employ N -acyl homoserine lactones (HSL) as AIs that are detected by LuxR-type QS receptors. Phage ARM81ld is a prophage of the aquatic bacterium Aeromonas sp. ARM81, and it encodes a homolog of a bacterial LuxR, called LuxR ARM81ld . LuxR ARM81ld detects host Aeromonas -produced C4-HSL, and in response, activates the phage lytic program, triggering death of its host and release of viral particles. Here, we show that phage LuxR ARM81ld activity is modulated by noncognate HSL ligands and by a synthetic small molecule inhibitor. We determine that HSLs with acyl chain lengths equal to or longer than C8 antagonize LuxR ARM81ld . For example, the C8-HSL AI produced by Vibrio fischeri that coexists with Aeromonads in aquatic environments, binds to and inhibits LuxR ARM81ld , and consequently, protects the host from lysis. Coculture of V. fischeri with the Aeromonas sp. ARM81 lysogen suppresses phage ARM81ld virion production. We propose that the cell density and species composition of the bacterial community could determine outcomes in bacterial-phage partnerships. 

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4. The value of information gathering in phage–bacteria warfare

   https://doi.org/10.1093/pnasnexus/pgad431  

   Dahan, Yuval; Wingreen, Ned S.; Meir, Yigal; Bahar, ed., Ivet (January 2024, PNAS Nexus)

   Abstract Phages—viruses that infect bacteria—have evolved over billions of years to overcome bacterial defenses. Temperate phage, upon infection, can “choose” between two pathways: lysis—in which the phage create multiple new phage particles, which are then liberated by cell lysis, and lysogeny—where the phage’s genetic material is added to the bacterial DNA and transmitted to the bacterial progeny. It was recently discovered that some phages can read information from the environment related to the density of bacteria or the number of nearby infection attempts. Such information may help phage make the right choice between the two pathways. Here, we develop a theoretical model that allows an infecting phage to change its strategy (i.e. the ratio of lysis to lysogeny) depending on an outside signal, and we find the optimal strategy that maximizes phage proliferation. While phages that exploit extra information naturally win in competition against phages with a fixed strategy, there may be costs to information, e.g. as the necessary extra genes may affect the growth rate of a lysogen or the burst size of new phage for the lysis pathway. Surprisingly, even when phages pay a large price for information, they can still maintain an advantage over phages that lack this information, indicating the high benefit of intelligence gathering in phage–bacteria warfare. 

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5. The landscape of lysogeny across microbial community density, diversity and energetics

   https://doi.org/10.1111/1462-2920.15640  

   Silveira, Cynthia_B; Luque, Antoni; Rohwer, Forest (June 2021, Environmental Microbiology)

   Summary Lysogens are common at high bacterial densities, an observation that contrasts with the prevailing view of lysogeny as a low‐density refugium strategy. Here, we review the mechanisms regulating lysogeny in complex communities and show that the additive effects of coinfections, diversity and host energic status yield a bimodal distribution of lysogeny as a function of microbial densities. At high cell densities (above 10⁶ cells ml⁻¹or g⁻¹) and low diversity, coinfections by two or more phages are frequent and excess energy availability stimulates inefficient metabolism. Both mechanisms favour phage integration and characterize the Piggyback‐the‐Winner dynamic. At low densities (below 10⁵ cells ml⁻¹or g⁻¹), starvation represses lytic genes and extends the time window for lysogenic commitment, resulting in a higher frequency of coinfections that cause integration. This pattern follows the predictions of the refugium hypothesis. At intermediary densities (between 10⁵and 10⁶ cells ml⁻¹or g⁻¹), encounter rates and efficient energy metabolism favour lysis. This may involve Kill‐the‐Winner lytic dynamics and induction. Based on these three regimes, we propose a framework wherein phage integration occurs more frequently at both ends of the host density gradient, with distinct underlying molecular mechanisms (coinfections and host metabolism) dominating at each extreme. 

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