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Growth of Magnetotactic Sulfate‐Reducing Bacteria in Oxygen

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Growth of Magnetotactic Sulfate‐Reducing Bacteria in Oxygen Environmental Microbiology Reports (2016) 8(6), 1003–1015 doi:10.1111/1758-2229.12479 Growth of magnetotactic sulfate-reducing bacteria in oxygen concentration gradient medium 1 2 Christopher T. Lefe`vre, * Paul A. Howse, D. magneticus is capable of aerobic growth with O2 Marian L. Schmidt,3 Monique Sabaty,1 as a terminal electron acceptor. This is the first report Nicolas Menguy,4 George W. Luther III5 and of consistent, reproducible aerobic growth of SRB. Dennis A. Bazylinski2** This finding is critical in determining important eco- 1CNRS/CEA/Aix-Marseille Universite UMR7265 Institut logical roles SRB play in the environment. Interest- de biosciences et biotechnologies Laboratoire de ingly, the crystal structure of the magnetite crystals Bioenerg etique Cellulaire, Saint Paul lez Durance, of D. magneticus grown under microaerobic condi- 13108, France. tions showed significant differences compared with 2School of Life Sciences, University of Nevada at Las those produced anaerobically providing more evi- Vegas, Las Vegas, NV, 89154-4004, USA. dence that environmental parameters influence mag- 3Department of Ecology and Evolutionary Biology, netosome formation. University of Michigan, Ann Arbor, MI, USA. 4Institut de Mineralogie, de Physique des Materiaux et de Cosmochimie, Sorbonne Universites, Universite Introduction Pierre et Marie Curie, UMR 7590 CNRS, Institut de Dissimilatory sulfate-reducing bacteria (SRB) are gener- Recherche pour le Developpement UMR 206, Museum ally considered to be strict anaerobes regarding growth National d’Histoire Naturelle, Paris Cedex 05, 75252, (Rabus et al., 2013). Widespread in marine and fresh- France. water sediments, they constitute a morphologically and 5School of Marine Science and Policy, University of metabolically diverse group of prokaryotes, phylogeneti- Delaware, 700 Pilottown Rd. Lewes, DE, 19958, USA cally belonging to both the Bacteria and Archaea domains, and able to use a wide variety of organic com- Summary pounds. SRB obtain energy for cell synthesis and growth by coupling the oxidation of these organic com- Although dissimilatory sulfate-reducing bacteria pounds or molecular hydrogen (H ) to the reduction of (SRB) are generally described as strictly anaerobic 2 sulfate (SO22) to sulfide (H S, HS2) (Rabus et al., organisms with regard to growth, several reports 4 2 2013). have shown that some SRB, particularly Desulfovi- Most known SRB belong to the Deltaproteobacteria brio species, are quite resistant to O . For example, 2 class of the Proteobacteria phylum in the domain Bacte- SRB remain viable in many aerobic environments ria. Those in the genus Desulfovibrio were described as while some even reduce O to H O. However, repro- 2 2 strictly anaerobic bacteria since their discovery more ducible aerobic growth of SRB has not been unequiv- than 100 years ago (Beijerinck, 1895). D. vulgaris and ocally documented. Desulfovibrio magneticus is a D. desulfuricans were used for many years as model SRB that is also a magnetotactic bacterium (MTB). organisms to study sulfate reduction (Voordouw and MTB biomineralize magnetosomes which are intracel- Wall, 1993). Dissimilatory SRB are often present in bio- lular, membrane-bounded, magnetic iron mineral topes where they are exposed to oxic conditions and crystals. The ability of D. magneticus to grow aerobi- some have even been shown to be metabolically active cally in several different media under air where an O 2 in microaerobic environments (Hardy and Hamilton, concentration gradient formed, or under O -free N 2 2 1981; Battersby et al., 1985; Sass et al., 1996; 1997; gas was tested. Under air, cells grew as a microaero- Krekeler et al., 1997; Sass et al., 1998; Lobo et al., philic band of cells at the oxic–anoxic interface in 2007) showing that these bacteria are quite resistant to media lacking sulfate. These results show that O2 (Cypionka et al., 1985; Sass et al., 1996; 1997; 1998; Krekeler et al., 1997). Some SRB not only survive exposure to O2 for at least days, but some even reduce *For correspondence. *E-mail [email protected]; Tel. 133 4 42 25 32 93. **E-mail [email protected]; O2 to H2O (Dannenberg et al., 1992), coupling aerobic Tel. 101-702-895-5832; Fax 101 702 895 3956. respiration to ATP formation (Dilling and Cypionka, 1990; VC 2016 Society for Applied Microbiology and John Wiley & Sons Ltd 1004 C. T. Lefe`vre et al. Cypionka, 2000) driving O2-dependent enhancement of and exhibit specific arrangements within the cell. These growth (Sigalevich et al., 2000). Johnson et al. reported features indicate that the formation of magnetosomes by aerobic growth of D. vulgaris Hildenborough although MTB is under precise biological control. Phylogenetic growth was meagre at best if even present (Johnson analysis shows that there is an important correlation et al., 1997). between the composition and morphology of the magne- To counteract the deleterious effects of highly reactive tosome mineral crystals produced by MTB and their derivatives of O2, many anaerobic organisms developed phylogenetic affiliation (Abreu et al., 2011; Lefe`vre et al., defense systems similar to those found in aerobes 2011a,b, 2012, 2013). Magnetotactic Alpha- and Gam- (Storz et al., 1990; Dolla et al., 2006). Despite the maproteobacteria, the later-diverging classes of the Pro- capacity of some SRB to couple O2 reduction with ener- teobacteria, biomineralize morphologically consistent, gy conservation, the observed chemotaxis of some spe- well-defined crystals of magnetite that include cubocta- cies toward microaerobic zones, and the detoxification hedral and elongated prisms (Devouard et al., 1998; mechanisms developed by some strains, consistent, Lefe`vre et al., 2012). In contrast, in the magnetotactic reproducible aerobic growth by SRB for an infinite num- Deltaproteobacteria, the most deeply diverging group of ber of generations has never been observed (Cypionka, the Proteobacteria, that biomineralize magnetite, grei- 2000; Dolla et al., 2006; Rabus et al., 2013). Other alter- gite, or both, the magnetite crystals are always bullet- native terminal electron acceptors to sulfate are used by shaped. The magnetotactic Nitrospirae and Omnitroph- some SRB; for instance, inorganic sulfur species such ica, the more deeply branching phylogenetic groups that 22 22 as sulfite (SO3 ), thiosulfate (S2O3 ), trithionate contain MTB (Jogler et al., 2011; Kolinko et al., 2012), 22 22 22 (S3O6 ), tetrathionate (S4O6 ) and dithionite (S2O4 ) are known to biomineralize only magnetite crystals are respired by some Desulfovibrio species while sulfo- whose morphologies are very similar to those found in nates, dimethyl sulfoxide (DMSO), nitrate and nitrite are the Deltaproteobacteria (Lefe`vre et al., 2011a, b). Thus, also used by some SRB. Fumarate and malate are also based on the phylogeny of MTB and the type of magne- fermented by some Desulfovibrio species (Rabus et al., tosomes that they biomineralize, it has been suggested 2013). Thus there is no reason to assume that the that bullet-shaped magnetite crystals represent the first capacities for dissimilatory sulfate reduction and aerobic magnetosome mineral phase (Lefe`vre et al., 2013). In growth in the same bacterium are mutually exclusive. addition to the genetic control over the type of crystal Magnetotactic bacteria (MTB) biomineralize magneto- mineralized in the magnetosome membrane, environ- somes, intracellular membrane-enclosed magnetic crys- mental parameters also play a role in the regulation of tals, causing them to swim along the Earth’s magnetosome formation. For instance, it was shown geomagnetic field lines. MTB are ubiquitous in aquatic that rates of iron uptake change the morphology of mag- environments but are generally localized at the oxic– netite crystals (Faivre et al., 2008). Culturing experi- anoxic interface (OAI) (Bazylinski and Frankel, 2004). ments also showed that depending on environmental Magnetosomes appear to enhance aerotaxis by reduc- conditions, strain BW-1, preferentially mineralizes mag- ing a 3-dimensional search for the OAI to 1-dimension netite (high redox potential) or greigite (reduced condi- where cells swim up and down along the Earth’s inclined tions) as a function of the redox conditions (Lefe`vre geomagnetic field lines (Bazylinski and Frankel, 2004). et al., 2011a, b). MTB belong to three major groups of Gram-negative Here we show that some magnetotactic SRB of the prokaryotes including the Proteobacteria, Nitrospirae genus Desulfovibrio are capable of reproducible, consis- and Omnitrophica phyla (Bazylinski et al., 2013) and tent aerobic growth in semi-solid oxygen concentration possibly the candidate phylum Latescibacteria (Lin and gradient ([O2]-gradient) medium lacking sulfate. In such Pan, 2015) of the Fibrobacteres-Chlorobi-Bacteroidetes conditions, the magnetosomes present consistent mor- (FCB) superphylum (Rinke et al., 2013). Deltaproteobac- phological variations that could be used as biomarkers terial MTB reduce and grow with sulfate as a terminal to understand past environmental conditions present in electron acceptor (Bazylinski et al., 2013). The polyphy- geological records where such magnetosome morpholo- letic origin idea of magnetosome biomineralization arose gy was deposited. from the discovery of the first magnetotactic Deltapro- teobacteria, a multicellular magnetotactic prokaryote Results (DeLong et al., 1993), later found to likely be a SRB Isolation of magnetotactic SRB (Abreu et al., 2011). Other deltaproteobacterial sulfate-
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