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ABSTRACT Mpox disease, caused by the monkeypox virus (MPXV), was recently classified as a public health emergency of international concern due to its high lethality and pandemic potential. MPXV is a zoonotic disease that emerged and is primarily spread by small rodents. Historically, it was considered mainly zoonotic and not likely to sustain human-to-human transmission. However, the worldwide outbreak of Clade IIb MPXV from 2020 to 2022 and ongoing Clade I MPXV epidemics in the Democratic Republic of the Congo and surrounding areas are a warning that human-adapted MPXVs will continually arise. Understanding the viral genetic determinants of host range, pathogenesis, and immune evasion is imperative for developing control strategies and predicting the future of Mpox. Here, we delve into the MPXV genome to detail genes involved in host immune evasion strategies for this zoonotic rodent-borne and human-circulating virus. We compare MPXV gene content to related Orthopoxviruses, which have narrow host ranges, to identify potential genes involved in species-specific pathogenesis and host tropism. In addition, we cover the key virulence factor differences that distinguish the MPXV clade lineages. Finally, we dissect how genomic reduction of Orthopoxviruses, through various molecular mechanisms, is contributing to the generation of novel MPXV lineages with increased human adaptation. This review aims to highlight gene content that defines the MPXV species, MPXV clades, and novel MPXV lineages that have culminated in this virus being elevated to a public health emergency of national concern. 

ABSTRACT The field of microbial ecology, evolution, and biodiversity (EEB) is at the leading edge of understanding how microbes shape our biosphere and influence the well-being of humankind and Earth. To that end, EEB is developing new transdisciplinary tools to analyze these ecologically critical, complex microbial communities. The American Society for Microbiology’s Council on Microbial Sciences hosted a virtual retreat in 2023 to discuss the trajectory of EEB both within the Society and microbiology writ large. The retreat emphasized the interconnectedness of microbes and their outsized global influence on environmental and host health. The maximal potential impact of EEB will not be achieved without contributions from disparate fields that unite diverse technologies and data sets. In turn, this level of transdisciplinary efforts requires actively encouraging “broad” research, spanning inclusive global collaborations that incorporate both scientists and the public. Together, the American Society for Microbiology and EEB are poised to lead a paradigm shift that will result in a new era of collaboration, innovation, and societal relevance for microbiology. 

ABSTRACT Marine bacteria face a constant influx of new extracellular DNA (exDNA) due to the massive viral lysis that occurs in the ocean on a daily basis. Generally, biofilms have shown to be induced by self-secreted exDNA. However, the effect of various types of exDNA with varying lengths, self vs non-self, as well as guanine-cytosine content (GC) content on biofilm formation has not been explored, despite being a critical component of the extracellular polymeric substance. To test the effect of such exDNA on biofilms, a marine bioluminescent bacterium (Vibrio hyugaensis) was isolated from the Sippewissett Salt Marsh, USA, and treated with various types of exDNA. We observed rapid pellicle formation with distinct morphologies only in cultures treated with herring sperm gDNA, anotherVibriospp. gDNA, and an oligomer of 61–80% GC content. With pH measurements before and after the treatment, we observed a positive correlation between biofilm formation and the change to a more neutral pH. Our study highlights the importance of studying DNA-biofilm interaction by carefully examining the physical properties of the DNA and by varying its content, length, and source. Our observation may serve as the basis for future studies that seek to interrogate the molecular explanation for the various types of exDNA and their effects on biofilm formation. IMPORTANCEBacteria mostly exist as biofilm, a protective niche that promotes protection from the environment and nutrient uptake. By forming these structures, bacteria have caused recalcitrant antibiotic-resistant infections, contamination of dairy and seafood, and fouling equipment in the industry. A critical component that makes up the extracellular polymeric substances, the structural component of a biofilm, is the extracellular DNA secreted by the bacteria found in the biofilm. However, previous studies on DNA and biofilm formation have neglected the unique properties of nucleic acid and its high diversity. Our study aims at disentangling these DNA properties by monitoring their effect at inducing biofilm formation. By varying length, self vs non-self, and GC percentage, we used various microscopy techniques to visualize the structural composition of aVibrio hyugaensisbiofilm. We observed DNA-dependent biofilm stimulation in this organism, a novel function of DNA in biofilm biology. 

ABSTRACT The effort to discover novel phages infecting Staphylococcus epidermidis contributes to both the development of phage therapy and the expansion of genome-based phage phylogeny. Here, we report the genome of an S. epidermidis -infecting phage, Lacachita, and compare its genome with those of five other phages with high sequence identity. These phages represent a novel siphovirus genus, which was recently reported in the literature. The published member of this group was favorably evaluated as a phage therapeutic agent, but Lacachita is capable of transducing antibiotic resistance and conferring phage resistance to transduced cells. Members of this genus may be maintained within their host as extrachromosomal plasmid prophages, through stable lysogeny or pseudolysogeny. Therefore, we conclude that Lacachita may be temperate and members of this novel genus are not suitable for phage therapy. IMPORTANCE This project describes the discovery of a culturable bacteriophage infecting Staphylococcus epidermidis that is a member of a rapidly growing novel siphovirus genus. A member of this genus was recently characterized and proposed for phage therapy, as there are few phages currently available to treat S. epidermidis infections. Our data contradict this, as we show Lacachita is capable of moving DNA from one bacterium to another, and it may be capable of maintaining itself in a plasmid-like state in infected cells. These phages’ putative plasmid-like extrachromosomal state appears to be due to a simplified maintenance mechanism found in true plasmids of Staphylococcus and related hosts. We suggest Lacachita and other identified members of this novel genus are not suitable for phage therapy. 

ABSTRACT Within social insect colonies, microbiomes often differ between castes due to their different functional roles and between colony locations. Trachymyrmex septentrionalis fungus-growing ants form colonies throughout the eastern United States and northern Mexico that include workers, female and male alates (unmated reproductive castes), larvae, and pupae. How T. septentrionalis microbiomes vary across this geographic range and between castes is unknown. Our sampling of individual ants from colonies across the eastern United States revealed a conserved T. septentrionalis worker ant microbiome and revealed that worker ant microbiomes are more conserved within colonies than between them. A deeper sampling of individual ants from two colonies that included all available castes (pupae, larvae, workers, and female and male alates), from both before and after adaptation to controlled laboratory conditions, revealed that ant microbiomes from each colony, caste, and rearing condition were typically conserved within but not between each sampling category. Tenericute bacterial symbionts were especially abundant in these ant microbiomes and varied widely in abundance between sampling categories. This study demonstrates how individual insect colonies primarily drive the composition of their microbiomes and shows that these microbiomes are further modified by developmental differences between insect castes and the different environmental conditions experienced by each colony. IMPORTANCE This study investigates microbiome assembly in the fungus-growing ant Trachymyrmex septentrionalis , showing how colony, caste, and lab adaptation influence the microbiome and revealing unique patterns of mollicute symbiont abundance. We find that ant microbiomes differ strongly between colonies but less so within colonies. Microbiomes of different castes and following lab adaptation also differ in a colony-specific manner. This study advances our understanding of the nature of individuality in social insect microbiomes and cautions against the common practice of only sampling a limited number of populations to understand microbiome diversity and function. 

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. 

ABSTRACT The degree to which independent populations subjected to identical environmental conditions evolve in similar ways is a fundamental question in evolution. To address this question, microbial populations are often experimentally passaged in a given environment and sequenced to examine the tendency for similar mutations to repeatedly arise. However, there remains the need to develop an appropriate statistical framework to identify genes that acquired more mutations in one environment than in another (i.e., divergent evolution), genes that serve as genetic candidates of adaptation. Here, we develop a mathematical model to evaluate evolutionary outcomes among replicate populations in the same environment (i.e., parallel evolution), which can then be used to identify genes that contribute to divergent evolution. Applying this approach to data sets from evolve-and-resequence experiments, we found that the distribution of mutation counts among genes can be predicted as an ensemble of independent Poisson random variables with zero free parameters. Building on this result, we propose that the degree of divergent evolution at a given gene between populations from two different environments can be modeled as the difference between two Poisson random variables, known as the Skellam distribution. We then propose and apply a statistical test to identify specific genes that contribute to divergent evolution. By focusing on predicting patterns among replicate populations in a given environment, we are able to identify an appropriate test for divergence between environments that is grounded in first principles. IMPORTANCE There is currently no universally accepted framework for identifying genes that contribute to molecular divergence between microbial populations in different environments. To address this absence, we developed a null model to describe the distribution of mutation counts among genes. We find that divergent evolution within a given gene can be modeled as the absolute difference in the total number of mutations observed between two environments. This quantity is effectively captured by a probability distribution known as the Skellam distribution, providing an appropriate statistical test for researchers seeking to identify the set of genes that contribute to divergent evolution in microbial evolution experiments. 

ABSTRACT Human infection challenge studies involving the intentional infection of research participants with a disease-causing agent have recently been suggested as a means to speed up the search for a vaccine for the ongoing coronavirus disease 2019 (COVID-19) outbreak. Calls for challenge studies, however, rely on the expected social value of these studies. This value represents more than the simple possibility that a successful study will lead to the rapid development and dissemination of vaccines but also some expectation that this will actually occur. I show how this expectation may not be realistic in the current political moment and offer potential ways to make sure that any challenge trials that arise actually achieve their goals.