Upon nutrient depletion, bacteria stop proliferating and undergo physiological and morphological changes to ensure their survival. Yet, how these processes are coordinated in response to distinct starvation conditions is poorly understood. Here we compare the cellular responses of Caulobacter crescentus to carbon (C), nitrogen (N) and phosphorus (P) starvation conditions. We find that DNA replication initiation and abundance of the replication initiator DnaA are, under all three starvation conditions, regulated by a common mechanism involving the inhibition of DnaA translation. By contrast, cell differentiation from a motile swarmer cell to a sessile stalked cell is regulated differently under the three starvation conditions. During C and N starvation, production of the signaling molecules (p)ppGpp is required to arrest cell development in the motile swarmer stage. By contrast, our data suggest that low (p)ppGpp levels under P starvation allow P-starved swarmer cells to differentiate into sessile stalked cells. Further, we show that limited DnaA availability, and consequently absence of DNA replication initiation, is the main reason that prevents P-starved stalked cells from completing the cell cycle. Together, our findings demonstrate that C. crescentus decouples cell differentiation from DNA replication initiation under certain starvation conditions, two otherwise intimately coupled processes. We hypothesize that arresting the developmental program either as motile swarmer cells or as sessile stalked cells improves the chances of survival of C. crescentus during the different starvation conditions.

Model bacteria are fundamental for research, but knowledge about their ecology and evolution is often limited. Here, we establish an evolutionary and ecological context for the model organism Caulobacter crescentus—an alphaproteobacterium intensively studied for its dimorphic lifecycle. By analyzing the phylogenetic relatedness and genetic potential of hundreds of Caulobacterales species, we reveal substantial diversity regarding their environmental distribution, morphology, cell development, and metabolism. Our work provides insights into the evolutionary history of morphological features such as the cell curvature determinant crescentin and uncovers a striking case of convergent loss of traits for cellular dimorphism among close relatives of C. crescentus. Moreover, we find that genes for phototrophy are widespread across Caulobacterales and that the new genus Acaudatibacter, described here, includes the first reported Caulobacterales lineage with photoautotrophic potential. Our study advances our understanding of an environmentally widespread bacterial order and sheds light on the evolution of fundamental prokaryotic features.

The Caulobacteraceae are a widespread family of environmental bacteria, including biodegraders, plant commensals, and opportunistic pathogens. Their type species, Caulobacter vibrioides (C. crescentus), is a key model organisms that has shaped our understanding of bacterial cell biology. Despite their ecological roles and importance for research, much of the Caulobacteraceae diversity remains undescribed. Here, we report the isolation and characterization of 58 Caulobacteraceae strains, including 15 new species from the genera Brevundimonas and Caulobacter. The new species display extensive diversity in genome organization, genetic potential, cell morphology and physiology. Importantly, we uncover features previously overlooked in this family, including quorum sensing pathways and lateral cell–cell interactions in biofilm formation, likely mediated by giant secreted adhesins. Our work provides cultured representatives of major Caulobacteraceae clades and thus substantially expands the known diversity of this ecologically and scientifically important bacterial family.

Plasmids are DNA molecules that replicate independently from chromosomes and often transfer themselves between host cells, facilitating the rapid spread of adaptive traits in bacterial populations. Plasmids have mostly been studied in bacteria with simple cell morphologies. However, we recently identified several natural plasmids among Caulobacteraceae species, a family of ubiquitous environmental bacteria notable for their complex lifecycles, posing questions on how these plasmids propagate themselves inside their asymmetrically reproducing hosts. Here, we characterize 28 complete Caulobacteraceae plasmids and their core propagation modules. We find that most are conjugative plasmids of iteron- and/or RepABC-types, and that the secondary chromosomes of Asticcacaulis species are chromids that derive from plasmids. Despite sharing conserved core propagation systems, we show that related Caulobacteraceae plasmids encode diverse accessory genes, including modules for synthesis of novel antimicrobial compounds and adaptation against stressors such as heavy metals, oxidative stress, DNA damage, and toxic hydrocarbons. Finally, our data suggest that Caulobacteraceae plasmids are coordinated with the cell developmental program of their dimorphic hosts, as indicated by widespread CtrA binding sites, plasmid-encoded GcrA homologs, and GANTC methylation motifs in origins and promoters of replication initiators genes. In sum, our study provides a comprehensive characterization of a previously overlooked group of plasmids and highlights their role in the adaptability and evolution of a bacterial family of both ecological and scientific importance.

Many bacteria have complex pleomorphic lifecycles — a feature particularly widespread across the class Alphaproteobacteria of the phylum Pseudomonadota. While research on bacteria with pleomorphic lifecycles has for many years focused on the dimorphic bacterium Caulobacter crescentus, more recent studies on less established alphaproteobacterial model bacteria have uncovered diverse variations of bacterial pleomorphism. Here, we provide an overview of the diversity and evolution of the complex lifecycles among dimorphic Alphaproteobacteria and highlight the presence of analogous lifecycles in unrelated bacteria across the bacterial domain. We discuss the commonalities and differences between dimorphic species, as well as the selective pressures that might have sculpted their lifecycles. Furthermore, we exemplify how the cellular appendages common among dimorphic Alphaproteobacteria, referred to as prosthecae, are not inherently linked to dimorphism. Finally, we highlight how the large diversity of dimorphic Alphaproteobacteria can be used to shed light onto the evolution of bacterial cell biology.