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Abstract Motivation: The study of bacterial genome dynamics is vital for understanding the mechanisms underlying microbial adaptation, growth, and their impact on host phenotype. Structural variants (SVs), genomic alterations of 50 base pairs or more, play a pivotal role in driving evolutionary processes and maintaining genomic heterogeneity within bacterial populations. While SV detection in isolate genomes is relatively straightforward, metagenomes present broader challenges due to the absence of clear reference genomes and the presence of mixed strains. In response, our proposed method rhea, forgoes reference genomes and metagenome-assembled genomes (MAGs) by encompassing all metagenomic samples in a series (time or other metric) into a single co-assembly graph. The log fold change in graph coverage between successive samples is then calculated to call SVs that are thriving or declining. Results: We show rhea to outperform existing methods for SV and horizontal gene transfer (HGT) detection in two simulated mock metagenomes, particularly as the simulated reads diverge from reference genomes and an increase in strain diversity is incorporated. We additionally demonstrate use cases for rhea on series metagenomic data of environmental and fermented food microbiomes to detect specific sequence alterations between successive time and temperature samples, suggesting host advantage. Our approach leverages previous work in assembly graph structural and coverage patterns to provide versatility in studying SVs across diverse and poorly characterized microbial communities for more comprehensive insights into microbial gene flux. Availability and implementation: rhea is open source and available at: https://github.com/treangenlab/rhea. 

Chloroflexus sp. MS-CIW-1 was isolated from a phototrophic mat in Mushroom Spring, an alkaline hot spring in Yellowstone National Park, WY, USA. We report the draft genome of 4.8 Mb consisting of 6 contigs with 3755 protein-coding genes and a GC content of 54.45%. 

Microbial phototrophic communities dominated early Earth and thrive to this day, particularly in extreme environments. We focus on the impact of diel oscillations on phototrophic biofilms, especially in hot springs, where oxygenic phototrophs are keystone species that use light energy to fix carbon and often nitrogen. They exhibit photo-motility and stratification, and alter the physicochemical environment by driving O2, CO2, and pH oscillations. Omics analyses reveal extensive genomic and functional diversity in biofilms, but linking this to a predictive understanding of their structure and dynamics remains challenging. This can be addressed by better spatiotemporal resolution of microbial interactions, improved tools for building and manipulating synthetic communities, and integration of empirical and theoretical approaches. 

ABSTRACT Phototrophic biofilms in most environments experience major changes in light levels throughout a diel cycle. Phototaxis can be a useful strategy for optimizing light exposure under these conditions, but little is known about its role in cyanobacteria from thermal springs. We examined two closely related Synechococcus isolates ( Synechococcus OS-A dominates at 60 to 65°C and OS-B′ at 50 to 55°C) from outflows of Octopus Spring in Yellowstone National Park. Both isolates exhibited phototaxis and photokinesis in white light, but with differences in speed and motility bias. OS-B′ exhibited phototaxis toward UVA, blue, green, and red wavelengths, while OS-A primarily exhibited phototaxis toward red and green. OS-A also exhibited negative phototaxis under certain conditions. The repertoires of photoreceptors and signal transduction elements in both isolates were quite different from those characterized in other unicellular cyanobacteria. These differences in the photoresponses between OS-A and OS-B′ in conjunction with in situ observations indicate that phototactic strategies may be quite versatile and finely tuned to the light and local environment. IMPORTANCE Optimizing light absorption is of paramount importance to photosynthetic organisms. Some photosynthetic microbes have evolved a sophisticated process called phototaxis to move toward or away from a light source. In many hot springs in Yellowstone National Park, cyanobacteria thrive in thick, laminated biofilms or microbial mats, where small movements can result in large changes in light exposure. We quantified the light-dependent motility behaviors in isolates representing two of the most abundant and closely related cyanobacterial species from these springs. We found that they exhibited unexpected differences in their speed, directionality, and responses to different intensities or qualities of light. An examination of their genomes revealed several variations from well-studied phototaxis-related genes. Studying these recently isolated cyanobacteria reveals that diverse phototactic strategies can exist even among close relatives in the same environment. It also provides insights into the importance of phototaxis for growth and survival in microbial biofilm communities. 

Primary endosymbiosis allowed the evolution of complex life on Earth. In this process, a prokaryote was engulfed and retained in the cytoplasm of another microbe, where it developed into a new organelle (mitochondria and plastids). During organelle evolution, genes from the endosymbiont are transferred to the host nuclear genome, where they must become active despite differences in the genetic nature of the “partner” organisms. Here, we show that in the amoebaPaulinella micropora, which harbors a nascent photosynthetic organelle, the “copy-paste” mechanism of retrotransposition allowed domestication of endosymbiont-derived genes in the host nuclear genome. This duplication mechanism is widespread in eukaryotes and may be a major facilitator for host–endosymbiont integration and the evolution of organelles. 

ABSTRACT Cyanobacteria rely on photosynthesis, and thus have evolved complex responses to light. These include phototaxis, the ability of cells to sense light direction and move towards or away from it. Analysis of mutants has demonstrated that phototaxis requires the coordination of multiple photoreceptors and signal transduction networks. The output of these networks is relayed to type IV pili (T4P) that attach to and exert forces on surfaces or other neighboring cells to drive “twitching” or “gliding” motility. This, along with the extrusion of polysaccharides or “slime” by cells, facilitates the emergence of group behavior. We evaluate recent models that describe the emergence of collective colony-scale behavior from the responses of individual, interacting cells. We highlight the advantages of “active matter” approaches in the study of bacterial communities, discussing key differences between emergent behavior in cyanobacterial phototaxis and similar behavior in chemotaxis or quorum sensing. 

Metagenomes encode an enormous diversity of proteins, reflecting a multiplicity of functions and activities. Exploration of this vast sequence space has been limited to a comparative analysis against reference microbial genomes and protein families derived from those genomes. Here, to examine the scale of yet untapped functional diversity beyond what is currently possible through the lens of reference genomes, we develop a computational approach to generate reference-free protein families from the sequence space in metagenomes. We analyze 26,931 metagenomes and identify 1.17 billion protein sequences longer than 35 amino acids with no similarity to any sequences from 102,491 reference genomes or the Pfam database. Using massively parallel graph-based clustering, we group these proteins into 106,198 novel sequence clusters with more than 100 members, doubling the number of protein families obtained from the reference genomes clustered using the same approach. We annotate these families on the basis of their taxonomic, habitat, geographical, and gene neighborhood distributions and, where sufficient sequence diversity is available, predict protein three-dimensional models, revealing novel structures. Overall, our results uncover an enormously diverse functional space, highlighting the importance of further exploring the microbial functional dark matter.