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Swarming bacteria are challenged by the need to invade hostile environments. Swarms of the flagellated bacterium Paenibacillus vortex can collectively transport other microorganisms. Here we show that P. vortex can invade toxic environments by carrying antibiotic-degrading bacteria; this transport is mediated by a specialized, phenotypic subpopulation utilizing a process not dependent on cargo motility. Swarms of beta-lactam antibiotic (BLA)-sensitive P. vortex used beta-lactamase-producing, resistant, cargo bacteria to detoxify BLAs in their path. In the presence of BLAs, both transporter and cargo bacteria gained from this temporary cooperation; there was a positive correlation between BLA resistance and dispersal. P. vortex transported only the most beneficial antibiotic-resistant cargo (including environmental and clinical isolates) in a sustained way. P. vortex displayed a bet-hedging strategy that promoted the colonization of nontoxic niches by P. vortex alone; when detoxifying cargo bacteria were not needed, they were lost. This work has relevance for the dispersal of antibiotic-resistant microorganisms and for strategies for asymmetric cooperation with agricultural and medical implications., IMPORTANCE Antibiotic resistance is a major health threat. We show a novel mechanism for the local spread of antibiotic resistance. This involves interactions between different bacteria: one species provides an enzyme that detoxifies the antibiotic (a sessile cargo bacterium carrying a resistance gene), while the other (Paenibacillus vortex) moves itself and transports the cargo. P. vortex used a bet-hedging strategy, colonizing new environments alone when the cargo added no benefit, but cooperating when the cargo was needed. This work is of interest in an evolutionary context and sheds light on fundamental questions, such as how environmental antibiotic resistance may lead to clinical resistance and also microbial social organization, as well as the costs, benefits, and risks of dispersal in the environment.

Summary Bacteria often use sophisticated cooperative behaviours, such as the development of complex colonies, elaborate biofilms and advanced dispersal strategies, to cope with the harsh and variable conditions of natural habitats, including the presence of antibiotics. Paenibacillus vortex uses swarming motility and cell-to-cell communication to form complex, structured colonies. The modular organization of P. vortex colony has been found to facilitate its dispersal on agar surfaces. The current study reveals that the complex structure of the colony is generated by the coexistence and transition between two morphotypes – ‘builders’ and ‘explorers’ – with distinct functions in colony formation. Here, we focused on the explorers, which are highly motile and spearhead colonial expansion. Explorers are characterized by high expression levels of flagellar genes, such as flagellin (hag), motA, fliI, flgK and sigD, hyperflagellation, decrease in ATP (adenosine-5′-triphosphate) levels, and increased resistance to antibiotics. Their tolerance to many antibiotics gives them the advantage of translocation through antibiotics-containing areas. This work gives new insights on the importance of cell differentiation and task distribution in colony morphogenesis and adaptation to antibiotics.

Background The pattern-forming bacterium Paenibacillus vortex is notable for its advanced social behavior, which is reflected in development of colonies with highly intricate architectures. Prior to this study, only two other Paenibacillus species (Paenibacillus sp. JDR-2 and Paenibacillus larvae) have been sequenced. However, no genomic data is available on the Paenibacillus species with pattern-forming and complex social motility. Here we report the de novo genome sequence of this Gram-positive, soil-dwelling, sporulating bacterium. Results The complete P. vortex genome was sequenced by a hybrid approach using 454 Life Sciences and Illumina, achieving a total of 289× coverage, with 99.8% sequence identity between the two methods. The sequencing results were validated using a custom designed Agilent microarray expression chip which represented the coding and the non-coding regions. Analysis of the P. vortex genome revealed 6,437 open reading frames (ORFs) and 73 non-coding RNA genes. Comparative genomic analysis with 500 complete bacterial genomes revealed exceptionally high number of two-component system (TCS) genes, transcription factors (TFs), transport and defense related genes. Additionally, we have identified genes involved in the production of antimicrobial compounds and extracellular degrading enzymes. Conclusions These findings suggest that P. vortex has advanced faculties to perceive and react to a wide range of signaling molecules and environmental conditions, which could be associated with its ability to reconfigure and replicate complex colony architectures. Additionally, P. vortex is likely to serve as a rich source of genes important for agricultural, medical and industrial applications and it has the potential to advance the study of social microbiology within Gram-positive bacteria.

Bacterial swarming resulting in collective navigation over surfaces provides a valuable example of cooperative colonization of new territories. The social bacterium Paenibacillus vortex exhibits successful and diverse swarming strategies. When grown on hard agar surfaces with peptone, P. vortex develops complex colonies of vortices (rotating bacterial aggregates). In contrast, during growth on Mueller?Hinton broth gelled into a soft agar surface, a new strategy of multi-level organization is revealed: the colonies are organized into a special network of swarms (or ?snakes? of a fraction of millimeter in width) with intricate internal traffic. More specifically, cell movement is organized in two or three lanes of bacteria traveling between the back and the front of the swarm. This special form of cellular logistics suggests new methods in which bacteria can share resources and risk while searching for food or migrating into new territories. While the vortices-based organization on hard agar surfaces has been modeled before, here, we introduce a new multi-agent bacterial swarming model devised to capture the swarms-based organization on soft surfaces. We test two putative generic mechanisms that may underlie the observed swarming logistics: (i) chemo-activated taxis in response to chemical cues and (ii) special align-and-push interactions between the bacteria and the boundary of the layer of lubricant collectively generated by the swarming bacteria. Using realistic parameters, the model captures the observed phenomena with semi-quantitative agreement in terms of the velocity as well as the dynamics of the swarm and its envelope. This agreement implies that the bacteria interactions with the swarm boundary play a crucial role in mediating the interplay between the collective movement of the swarm and the internal traffic dynamics.