High-speed motility originates from cooperatively pushing and pulling flagella bundles in bilophotrichous bacteria

Abstract

19Bacteria propel and change direction by rotating long, helical filaments, called flagella. The 20 number of flagella, their arrangement on the cell body and their sense of rotation 21 hypothetically determine the locomotion characteristics of a species. The movement of the 22 most rapid microorganisms has in particular remained unexplored because of additional 23 experimental limitations. We show that magnetotactic cocci with two flagella bundles on 24 one pole swim faster than 500 µm·s -1 along a double helical path, making them one of the 25 fastest natural microswimmers. We additionally reveal that the cells reorient in less than 5 26 ms, an order of magnitude faster than reported so far for any other bacteria. Using 27 hydrodynamic modeling, we demonstrate that a mode where a pushing and a pulling bundle 28 cooperate is the only possibility to enable both helical tracks and fast reorientations. The 29 advantage of sheathed flagella bundles is the high rigidity, making high swimming speeds 30 possible. 31 32 Introduction 33The understanding of microswimmer motility has implications ranging from the 34 comprehension of phytoplankton migration to the autonomously acting microbots in 35 medical scenarios [1, 2]. The most present microswimmers in our daily lives are bacteria, 36 most of which use flagella for locomotion. Well-studied examples of swimming 37 microorganisms include the peritrichous (several flagella all over the body surface) 38Escherichia coli with an occasionally distorted hydrodynamic flagella bundling [3] and the 39 monotrichous (one polar flagellum) Vibrio alginolyticus, which are pushed or pulled by a 40 flagellum and exploit a mechanical buckling instability to change direction [4, 5]. The 41 3 swimming speeds of so far studied cells are in the range of several 10 µm s -1 and their 42 reorientation events occur on the time scale of 50-100 ms [5, 6]. 43Magnetococcus marinus (MC-1) is a magnetotactic, spherical bacterium that is capable of 44 swimming extremely fast [7][8][9][10]. MC-1 as well as the closely related strain are 45 equipped with two bundles of flagella on one hemisphere (bilophotrichous cells). The 46 bacterium also features a magnetosome chain, which imparts the cell with a magnetic 47 moment ('magnetotactic' cell). They are assumed to swim with the cell body in front of both 48 flagella, which synchronously push the cell forward [7]. This assumption leads to helical 49 motion in the presence of a strong magnetic field, which exerts a torque on the cell's 50 magnetic moment, as seen in hydrodynamic simulations [12]. In the absence of a magnetic 51 field, this model predicts rather straight trajectories. 52Our observations disagree with the above-mentioned model, indicating that an 53 understanding of the physics of their swimming is still missing, even though proof of concept 54 biomedical applications of these bacteria have already emerged [2]. Here we show that MC-55 1 not only reach speeds of over 400 µm s -1 but that this speed is recorded along an 56 unexplored double he...

Origins of eukaryotic excitability

“…Importantly, most prokaryotes cannot steer deterministically in bulk fluid, nor is it advantageous to do so due to excessive rotational diffusion. Exceptions include a vibrioid bacterium [55], and magnetotatic bacteria including the bilophotrichous Magnetococcus marinus [330], and the multicellular magnetotactic prokaryotes (MMPs; approx. 10 µm) [331].…”

Single-cell motion of magnetotactic bacteria in microfluidic confinement: interplay between surface interaction and magnetic torque

“…It is The copyright holder for this preprint this version posted March 27, 2021. ; https://doi.org/10.1101/2021.03.27.437322 doi: bioRxiv preprint 3 allow the remote steering of microswimmers exhibiting a magnetic moment, a feature suitable for the remote control of the swimmers performing biomedical tasks in the human body 7 . Such microswimmers include magnetotactic bacteria [34][35][36] , i.e. bacteria equipped with a magnetic moment due to dedicated organelles, the magnetosomes, as well as biohybrid and synthetic magnetic swimmers 7,[37][38][39][40][41] .…”

“…Accordingly, a line of research has also developed, which seeks to understand the directionality of microswimmers and how to control them due to their tactic behaviors or due to interactions with external fields 8,32,33 This regard, magnetic fields are particularly interesting, as they allow the remote steering of microswimmers exhibiting a magnetic moment, a feature suitable for the remote control of the swimmers performing biomedical tasks in the human body 7 . Such microswimmers include magnetotactic bacteria 34–36 , i.e. bacteria equipped with a magnetic moment due to dedicated organelles, the magnetosomes, as well as biohybrid and synthetic magnetic swimmers 7,37–41 .…”

Bacterial flagellar motor as a multimodal biosensor

“…Bacteria are micron-scale organisms, usually swimming with speeds varying between tens and hundreds of body lengths per second [23,24,25,26], and thus, tracking them to measure their swimming velocity is not a trivial task. The efforts to do so can be broadly divided into measuring the single bacterium run speeds and tumbling rates [23, 27, 24, 28, 29][30, 31], and measuring the average speed of a bacterial population [32,33].…”