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In aerobic chemostat cultures maintained at 50% dissolved O2 tension (3.5 mg l−1 dissolved O2), Shewanella oneidensis strain MR-1 rapidly aggregated upon addition of 0.68 mM CaCl2 and retained this multicellular phenotype at high dilution rates. Confocal microscopy analysis of the extracellular matrix material contributing to the stability of the aggregate structures revealed the presence of extracellular DNA, protein and glycoconjugates. Upon onset of O2-limited growth (dissolved O2 below detection) however, the Ca2+-supplemented chemostat cultures of strain MR-1 rapidly disaggregated and grew as motile dispersed cells. Global transcriptome analysis comparing aerobic aggregated to O2-limited unaggregated cells identified genes encoding cell-to-cell and cell-to-surface adhesion factors whose transcription increased upon exposure to increased O2 concentrations. The aerobic aggregated cells also revealed increased expression of putative anaerobic electron transfer and homologues of metal reduction genes, including mtrD (SO1782), mtrE (SO1781) and mtrF (SO1780). Our data indicate that mechanisms involved in autoaggregation of MR-1 are dependent on the function of pilD gene which encodes a putative prepilin peptidase. Mutants of S. oneidensis strain MR-1 deficient in PilD and associated pathways, including type IV and Msh pili biogenesis, displayed a moderate increase in sensitivity to H2O2. Taken together, our evidence indicates that aggregate formation in S. oneidensis MR-1 may serve as an alternative or an addition to biochemical detoxification to reduce the oxidative stress associated with production of reactive oxygen species during aerobic metabolism while facilitating the development of hypoxic conditions within the aggregate interior. [ABSTRACT FROM AUTHOR]

This manuscript is dedicated to our friend, mentor, and coauthor Dr Terry Beveridge, who devoted his scientific career to advancing fundamental aspects of microbial ultrastructure using innovative electron microscopic approaches. During his graduate studies with Professor Robert Murray, Terry provided some of the first glimpses and structural evaluations of the regular surface arrays (S-layers) of Gram-negative bacteria ( Beveridge & Murray, 1974 , 1975 , 1976a ). Beginning with his early electron microscopic assessments of metal binding by cell walls from Gram-positive bacteria ( Beveridge & Murray, 1976b , 1980 ) and continuing with more than 30 years of pioneering research on microbe–mineral interactions ( Hoyle & Beveridge, 1983 , 1984 ; Ferris et al., 1986 ; Gorby et al., 1988 ; Beveridge, 1989 ; Mullen et al., 1989 ; Urrutia Mera et al., 1992 ; Mera & Beveridge, 1993 ; Brown et al., 1994 ; Konhauser et al., 1994 ; Beveridge et al., 1997 ; Newman et al., 1997 ; Lower et al., 2001 ; Glasauer et al., 2002 ; Baesman et al., 2007 ), Terry helped to shape the developing field of biogeochemistry. Terry and his associates are also widely regarded for their research defining the structure and function of outer membrane vesicles from Gram-negative bacteria that facilitate processes ranging from the delivery of pathogenic enzymes to the possible exchange of genetic information. The current report represents the confluence of two of Terry's thematic research streams by demonstrating that membrane vesicles produced by dissimilatory metal-reducing bacteria from the genus Shewanella catalyze the enzymatic transformation and precipitation of heavy metals and radionuclides. Under low-shear conditions, membrane vesicles are commonly tethered to intact cells by electrically conductive filaments known as bacterial nanowires. The functional role of membrane vesicles and associated nanowires is not known, but the potential for mineralized vesicles that morphologically resemble nanofossils to serve as palaeontological indicators of early life on Earth and as biosignatures of life on other planets is recognized. [ABSTRACT FROM AUTHOR]