Shewanella oneidensis MR-1 chemotaxis proteins and electron-transport chain components essential for congregation near insoluble electron acceptors

Abstract

Shewanella oneidensis MR-1 cells utilize a behaviour response called electrokinesis to increase their speed in the vicinity of IEAs (insoluble electron acceptors), including manganese oxides, iron oxides and poised electrodes [Harris, El-Naggar, Bretschger, Ward, Romine, Obraztsova and Nealson (2010) Proc. Natl. Acad. Sci. U.S.A. 107, 326-331]. However, it is not currently understood how bacteria remain in the vicinity of the IEA and accumulate both on the surface and in the surrounding medium. In the present paper, we provide results indicating that cells that have contacted the IEAs swim faster than those that have not recently made contact. In addition, fast-swimming cells exhibit an enhancement of swimming reversals leading to rapid non-random accumulation of cells on, and adjacent to, mineral particles. We call the observed accumulation near IEAs 'congregation'. Congregation is eliminated by the loss of a critical gene involved with EET (extracellular electron transport) (cymA, SO_4591) and is altered or eliminated in several deletion mutants of homologues of genes that are involved with chemotaxis or energy taxis in Escherichia coli. These genes include chemotactic signal transduction protein (cheA-3, SO_3207), methyl-accepting chemotaxis proteins with the Cache domain (mcp_cache, SO_2240) or the PAS (Per/Arnt/Sim) domain (mcp_pas, SO_1385). In the present paper, we report studies of S. oneidensis MR-1 that lend some insight into how microbes in this group can 'sense' the presence of a solid substrate such as a mineral surface, and maintain themselves in the vicinity of the mineral (i.e. via congregation), which may ultimately lead to attachment and biofilm formation.

A dynamic periplasmic electron transfer network enables respiratory flexibility beyond a thermodynamic regulatory regime

“…The concept of transient electron storage is to some extent corroborated by results from Harris et al (2012). The authors observed a distinct response called electrokinesis when S. oneidensis cells were in the vicinity of an insoluble electron acceptor in the absence of oxygen.…”

A combined electrochemical and optical trapping platform for measuring single cell respiration rates at electrode interfaces

“…Despite the low cell density, it should be noted that we did not encounter difficulty finding cells in the vicinity of WEs, likely due to a previously reported phenomenon where cells congregate near insoluble electron acceptors. 39 Finally, this trapping culture is introduced into the chamber-chip assembly that is integrated into the optical trap.…”

The mechanisms of extracellular electron transfer

“…Further evidence to support the greater versatility of Shewanella is its motility [119,129], as opposed to Geobacter which is said to be non-motile [223]. This is reflected in the proteomic results presented in this thesis (sections 5.2.2 and 5.3.2) with the identification and quantification of flagellin related proteins present in S. oneidensis however absent in G. sulfurreducens.…”

“…The LB culture (3 ml) was used as an inoculum for 300 ml of defined minimal medium [119] that included lactate as the electron donor, a vitamin solution and oxygen and the electron acceptor. The culture was grown at 30 ˚C shaking at 200 rpm for 24 hours and then the cell density was adjusted to an OD600 of 0.6-0.7 and 5 ml was used as inoculum for each of the BES experiments that followed.…”

“…The triplicate BESs were rinsed with Milli Q and assembled under anaerobic conditions. Modified minimal medium [119] was used for all BES experiments with 18 mM lactate as the carbon and electron source. In all BES experiments the electrode was used as the electron accepter, therefore fumarate was omitted from the medium.…”