Redox Sensing within the Genus Shewanella.

Howard W Harris,Everett C Salas,Irene Sánchez-Andrea,Jeffrey S Mclean,Mohamed Y El-Naggar,Kenneth H Nealson,William Tran

doi:10.3389/fmicb.2017.02568

Abstract

A novel bacterial behavior called congregation was recently described in Shewanella oneidensis MR-1 as the accumulation of cells around insoluble electron acceptors (IEA). It is the result of a series of “run-and-reversal” events enabled by modulation of swimming speed and direction. The model proposed that the swimming cells constantly sense their surroundings with specialized outer membrane cytochromes capable of extracellular electron transport (EET). Up to this point, neither the congregation nor attachment behavior have been studied in any other strains. In this study, the wild type of S. oneidensis MR-1 and several deletion mutants as well as eight other Shewanella strains (Shewanella putrefaciens CN32, S. sp. ANA-3, S. sp. W3-18-1, Shewanella amazonensis SB2B, Shewanella loihica PV-4, Shewanella denitrificans OS217, Shewanella baltica OS155, and Shewanella frigidimarina NCIMB400) were screened for the ability to congregate. To monitor congregation and attachment, specialized cell-tracking techniques, as well as a novel cell accumulation after photo-bleaching (CAAP) confocal microscopy technique were utilized in this study. We found a strong correlation between the ability of strain MR-1 to accumulate on mineral surface and the presence of key EET genes such as mtrBC/omcA (SO_1778, SO_1776, and SO_1779) and gene coding for methyl-accepting protein (MCPs) with Ca+ channel chemotaxis receptor (Cache) domain (SO_2240). These EET and taxis genes were previously identified as essential for characteristic run and reversal swimming around IEA surfaces. CN32, ANA-3, and PV-4 congregated around both Fe(OH)3 and MnO2. Two other Shewanella spp. showed preferences for one oxide over the other: preferences that correlated with the metal content of the environments from which the strains were isolated: e.g., W3-18-1, which was isolated from an iron-rich habitat congregated and attached preferentially to Fe(OH)3, while SB2B, which was isolated from a MnO2-rich environment, preferred MnO2.

Highlights

In the late 1980’s, Shewanella oneidensis MR-1 (Myers and Nealson, 1988a) and later several species of Geobacter (Lovley et al, 1993; Champine et al, 2000) were shown to be capable of electron transfer to insoluble electron acceptors (IEAs), such as insoluble metal oxides and/or charged electrodes: a process called extracellular electron transport (EET) (Myers and Nealson, 1988b; Venkateswaran et al, 1999; Bond and Lovley, 2003)
Most of the early studies of energy taxis in MR-1 utilized a method of swarm plate assays (Nealson et al, 1995; Baraquet et al, 2009; Li et al, 2012)
Many Shewanella strains have been isolated from water column and sediment habitats in locations all across the globe

Summary

Introduction

In the late 1980’s, Shewanella oneidensis MR-1 (Myers and Nealson, 1988a) and later several species of Geobacter (Lovley et al, 1993; Champine et al, 2000) were shown to be capable of electron transfer to insoluble electron acceptors (IEAs), such as insoluble metal oxides and/or charged electrodes: a process called extracellular electron transport (EET) (Myers and Nealson, 1988b; Venkateswaran et al, 1999; Bond and Lovley, 2003). The congregation in response to IEA has only been studied for MR-1

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Results

Conclusion