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An Alphaproteobacterium Capable of Both Aerobic and Anaerobic Anoxygenic Photosynthesis but Incapable of Photoautotrophy: Charonomicrobium Ambiphototrophicum, Gen

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An Alphaproteobacterium Capable of Both Aerobic and Anaerobic Anoxygenic Photosynthesis but Incapable of Photoautotrophy: Charonomicrobium Ambiphototrophicum, Gen Photosynth Res (2011) 107:257–268 DOI 10.1007/s11120-011-9629-1 REGULAR PAPER An alphaproteobacterium capable of both aerobic and anaerobic anoxygenic photosynthesis but incapable of photoautotrophy: Charonomicrobium ambiphototrophicum, gen. nov., sp. nov. J. T. Csotonyi • E. Stackebrandt • J. Swiderski • P. Schumann • V. Yurkov Received: 13 September 2010 / Accepted: 20 January 2011 / Published online: 10 February 2011 Ó Springer Science+Business Media B.V. 2011 Abstract A facultatively aerobic deep brown coccoid to Keywords Charonomicrobium ambiphototrophicum Á ovoid bacterium, strain EG17T, was isolated from a saline AAP Á Aerobic anoxygenic phototorphs Á Anoxygenic effluent stream in the NaCl-dominated brine spring system photosynthesis Á Purple nonsulfur bacteria Á known as East German Creek in the province of Manitoba, Photoautotrophy Á Bacteriochlorophyll a Canada. The strain produced BChl a incorporated into a functional reaction center and two light-harvesting com- plexes with absorption peaks at 802, 850, and 879 nm. Introduction EG17T is the first reported anoxygenic phototroph capable of photoheterotrophic growth under both oxic and anoxic One of the most consistent dichotomies in microbiology is conditions. It yielded proportionally the greatest aerobic the segregation of aerobic and anaerobic photosynthesis photosynthetic biomass under oligotrophic conditions. The into different species of anoxygenic phototrophs. Purple results of 16S rRNA gene sequence comparisons revealed sulfur and nonsulfur bacteria (Proteobacteria), green sulfur that EG17T was related most closely to the aerobic an- bacteria (Chlorobi), green nonsulfur bacteria (Chloroflexi), oxygenic phototrophs Roseibacterium elongatum (98.3%) and heliobacteria (Firmicutes) all perform photosynthesis and quite distantly to both Dinoroseobacter shibae (95.2%) solely in the absence of oxygen. In sharp contrast, the more and Roseicyclus mahoneyensis (94.7%). The DNA G ? C recently discovered aerobic anoxygenic phototrophs (AAP) content was 65.6 mol%. On the basis of the unique dual synthesize and utilize an obligately aerobically functional aerobic/anaerobic photosynthetic capability, the distinctive photosynthetic apparatus (Rathgeber et al. 2004; Yurkov spectrophotometric absorption of the photosynthetic appa- and Csotonyi 2009). Possession of two photosystems (PS) ratus, diagnostic physiological and biochemical traits, and allows some cyanobacteria (e.g., Anabaena doliolum, the moderate phylogenetic separation between EG17T and Bhargava et al. 2008) to perform photosynthesis both aer- its nearest relatives, it is concluded that this microorganism obically (oxygenic, using both PS I and PS II) and anaer- should be classified as a novel genus and species, Charo- obically (anoxygenic, using only PS I). However, nomicrobium ambiphototrophicum gen. nov., sp. nov., with anoxygenic phototrophs, which have only a single photo- EG17T as the type strain. system, have never been reported to be capable of ener- getically harnessing light both in the presence and absence of oxygen. Strain EG17T is a rich brown anoxygenic phototroph & J. T. Csotonyi Á V. Yurkov ( ) that was isolated from the surface layers of a microbial mat Department of Microbiology, University of Manitoba, 418 Buller Building, Winnipeg, MB R3T 2N2, Canada (dominated by the marine green algae Percursaria per- e-mail: [email protected] cursa) in a runoff stream from a Canadian inland hyper- saline spring known as East German Creek (EGC; Csotonyi E. Stackebrandt Á J. Swiderski Á P. Schumann et al. 2008). These thalassohaline brine springs are more DSMZ-Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Inhoffenstrasse 7B, 38124 Braunschweig, than 600 km from the ocean, but achieve a salinity about Germany twice that of seawater (total dissolved solids 56.7–67.3%; 123 258 Photosynth Res (2011) 107:257–268 Csotonyi et al. 2008) by dissolution of salts from Devonian arabinose, bactopeptone, casamino acids, citrate, ethanol, marine sediments (Grasby 2000). Sulfate drives biogenic formate, fructose, glucose, glutamate, glycerol, glycolate, sulfide production in the subsurface sediments, supporting lactate, malate, methanol, propionate, pyruvate, succinate, anaerobic anoxygenic phototrophs in an illuminated zone sucrose, xylose, and yeast extract. Anaerobic carbon source at the surface of the sediments. Aerobic mat-like growth of preference was investigated in the light by adding singly cyanobacteria and green algae, chiefly P. percursa, overly the following carbon sources (1 g/l) to completely filled these communities (Csotonyi et al. 2008) was found in test tube cultures, using Na2S2O3 (0.5 g/l) as electron streams with flow rates of nearly 4,800 l/h (McKillop et al. donor: acetate, glutamate, lactate, malate, pyruvate, suc- 1992). Although AAP dominated the anoxygenic photo- cinate, and yeast extract. Photoautotrophy was tested aer- trophic community, constituting 15–36% of cultured bac- obically by measuring growth in the light in two serial teria, obligately anaerobic purple sulfur and nonsulfur transfers of liquid basal Medium A amended with 1.5 g/l bacteria related to Halochromatium glycolicum (strain NaHCO3 as carbon source and 0.5 g/l Na2S2O3 as electron EG18) and Roseospira marina (strain EG16), respectively, donor. Anaerobic photoautotrophy was assayed in dupli- also shared the habitat (Csotonyi et al. 2008). This obser- cate illuminated cultures of washed cells in stoppered and vation indicated that both aerobic and anaerobic micro- degassed test tubes of Medium A (4 and 8% NaCl) devoid habitats existed in close proximity to each other. of carbon sources except for (g/l): sodium bicarbonate (1.5) In this article, we describe the first phototrophic and either H2 (headspace gas), sodium thiosulfate (0.8) or organism possessing a single photosystem capable of per- sodium sulfide (0.12) as electron donor. A negative control forming both aerobic and anaerobic anoxygenic photo- (lacking bicarbonate and electron donors) and a positive synthesis. The results of this research underscore the great control (supplemented with 2 g/l yeast extract as carbon metabolic diversity of Proteobacteria, and are anticipated and electron donors) were also included. to stimulate further study of habitats with steep oxic gra- dients to isolate and study additional representatives of this DNA G ? C content determination and 16S rRNA unusually plastic physiological group. gene sequence analysis The DNA G ? C content was determined by using HPLC Materials and methods of nucleosides obtained according to Mesbah et al. (1989). For phylogenetic analysis, genomic DNA was extracted, Isolation and cultivation and the 16S rRNA gene sequence ([1,400 nucleotides long) was PCR-amplified and directly sequenced as stated EGC was sampled in May 2002 to enumerate the anoxy- by Rainey et al. (1996). Sequence reaction mixtures were genic phototrophic microbial community (Csotonyi et al. electrophoresed using a model 373A automatic DNA 2008). EG17T originated from within an algal mat with sequencer (Applied Biosystems). The sequences were 65.9% total dissolved solids and pH 6.9. The strain was aligned with published data obtained from the EMBL isolated from the subsurface of an agar deep containing nucleotide sequence database and the Ribosomal Database Medium B, designed for the enrichment of halophilic Project, using the ae2 editor (Maidak et al. 1999), and purple nonsulfur bacteria (Csotonyi et al. 2008), but was similarity values were determined. A neighbor-joining subsequently maintained aerobically on Medium A for dendrogram was reconstructed from a distance matrix AAP (Csotonyi et al. 2008). using the treeing algorithm of Felsenstein (1993). Boot- strap values were determined from 1,000 resamplings Morphological, physiological, and biochemical tests according to Felsenstein (1985). The sequence accession number AM691091 was obtained for EG17T. Morphology was examined in aerobic plate cultures on Medium A using a phase contrast microscope. Physiolog- Pigment analysis ical tests for salinity, temperature and pH tolerance, anti- biotic resistance, illuminated anaerobic growth with Presence of BChl a and carotenoids was assayed spectro- various electron donors, aerobic and anaerobic utilization photometrically in cultures that had been grown aerobically of organic carbon sources, fermentation, and presence of and anaerobically in the dark in liquid Medium A for lipase, gelatinase, catalase, and oxidase were determined as 5 days. Following centrifugation, pigments were extracted previously described (Yurkov et al. 1994). Aerobic organic from cells in acetone/methanol (7:2, v/v). Absorbance carbon utilization was tested in the dark using basal car- properties of pigments incorporated into the reaction center bon-free Medium A to which the following components (RC) and light-harvesting (LH) complexes were deter- were added singly at a concentration of 1 g/l: acetate, mined in vivo (cells resuspended in 0.1 M Tris-HCl buffer, 123 Photosynth Res (2011) 107:257–268 259 pH 7.8, and 30% bovine serum albumin), using a spec- trophotometer (U-2010; Hitachi), as previously described (Yurkov et al. 1994). Photosynthetic growth Growth of EG17T was measured (determined by the Bradford assay; Bradford 1976) under aerobic (30 ml cultures in 125-ml flasks) and anaerobic (completely filled 10-ml test tubes) conditions in the light (500 lux) and in the dark, on Medium B ? G, which was based on Medium B (Csotonyi et al. 2008) but supplemented with
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