Bacterial Biohybrid Microswimmers

Abstract

Over millions of years, Nature has optimized the motion of biological systems at the micro and nanoscales. Motor proteins to motile single cells have managed to overcome Brownian motion and solve several challenges that arise at low Reynolds numbers. In this review, we will briefly describe naturally motile systems and their strategies to move, starting with a general introduction that surveys a broad range of developments, followed by an overview about the physical laws and parameters that govern and limit motion at the microscale. We characterize some of the classes of biological microswimmers that have arisen in the course of evolution, as well as the hybrid structures that have been constructed based on these, ranging from Montemagno's ATPase motor to the SpermBot. Thereafter, we maintain our focus on bacteria and their biohybrids. We introduce the inherent properties of bacteria as a natural microswimmer and explain the different principles bacteria use for their motion. We then elucidate different strategies that have been employed for the coupling of a variety of artificial microobjects to the bacterial surface, and evaluate the different effects the coupled objects have on the motion of the "biohybrid." Concluding, we give a short overview and a realistic evaluation of proposed applications in the field.

Keywords: bacteriabots; bacterial motility; bacterial surface; binding; microswimmers; surface charge.

Figure 1

Schematic representation of natural and biohybrid swimmers on different length scales, showing how the characteristic swimmer velocity and Reynolds number changes with length scale. The classification of Bacterial biohybrid microswimmers according to the bacteria: object ratio is indicated; see the main text for details.

Figure 2

Bacterial locomotion. (A) Schematic (not to scale) structure of the flagellum in Gram-negative bacteria. OM, outer membrane; PG, peptidoglycan cell wall; CM, cytoplasmic membrane. Adapted from Madigan et al. (2014). (B) Different types of bacterial flagellation. (C) Different bacterial locomotion strategies: gliding (focal adhesion model) (adapted from Islam and Mignot, 2015), swarming (adapted from Kearns, 2010), and swimming. The direction of bacteria movement is indicated by black arrows. (D) Schematics (not to scale) of different swimming strategies. Run and tumble from Escherichia coli; forward, reverse, and turning by buckling of Vibrio alginolyticus (adapted from Son et al., 2013); stop and coil from Rhodobacter sphaeroides (adapted from Armitage and Macnab, ; Armitage et al., 1999); push, pull, and wrap from Pseudomonas putida (adapted from Hintsche et al., 2017). The direction of bacteria movement is indicated by the arrows. See main body text for details.

Figure 3

Schematic representation of different attachment strategies for the preparation of BacteriaBots.

Figure 4

Schematic representations and examples of the interaction of bacteria with variously shaped cargoes: (A) Single bacterium attached by optical trapping to a cuboid elongated zeolite L crystal (Barroso et al., 2015). (B,C) Preferential attachment of bacteria to spherical metal capped-PS Janus particles (Stanton et al., 2016) and Pluronic covered PS particles (Behkam and Sitti, 2008). (D) Bacteria attached to PS particles with different ellipsoidal body geometries (Sahari et al., 2012). (E) Bacteria captured inside a microtube regarding the bacteria driven microswimmer assembly (Stanton et al., 2017a). All images presented with corresponding copyright permissions.