Sedimenticola selenatireducens, gen. nov., sp. nov., an anaerobic selenate-respiring bacterium isolated from estuarine sediment

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Abstract

The respiration of selenate, as a terminal electron acceptor has been known for over a decade, but the microorganisms involved in this respiration are largely unknown. Here we characterize a novel selenate-respiring bacterium, strain AK4OH1, isolated from an estuarine sediment enrichment culture. Strain AK4OH1 has the unique capability to oxidize aromatic acids, such as benzoate, 4-hydroxybenzoate and 3-hydroxybenzoate, coupled to selenate respiration. This novel respiratory coupling has not been described before. Reduction of selenate is followed by stoichiometric accumulation of selenite. The strain grows in agar shake tubes forming bright red colonies due to precipitation of elemental selenium. Strain AK4OH1 is a strictly anaerobic bacterium, which can also respire nitrate and nitrite via denitrification. Analysis of the 16S rRNA gene sequence shows that this strain clusters with another selenate-reducing bacterium and a (per) chlorate reducing bacterium, within the Gammaproteobacteria, along with symbionts of bivalves and tubeworms. Based on its unique physiological capabilities and its 16S rRNA gene sequence phylogeny, we classify this strain AK4OH1 as a new genus and species with the proposed name Sedimenticola selenatireducens.

Introduction

Microbially mediated reduction of selenate and selenite has been known for sometime. A number of bacteria resist selenite toxicity by converting it to elemental selenium, which was first demonstrated by Shrift and Kelly [21]. This process is not coupled to growth and is a common mechanism to reduce the toxicity of the element similar to other metal resistance mechanisms that are prevalent in bacteria [6]. The microorganisms that carry out this process include Pseudomonas stutzeri that can aerobically transform up to 48 mM selenate or selenite to elemental selenium [14]. Although organisms such as Stenotrophomonas maltophilia [7], Wollinella succinogenes [24] and Desulfovibrio desulfuricans [25] cannot use selenium compounds as terminal electron acceptors for respiration, they can convert it to elemental selenium and may accumulate it inside or outside of the cell. Dissimilatory selenate reduction refers to a microbial sulfate independent anaerobic respiration where selenate is reduced to selenite and further to elemental selenium [19]. This process is one of the major sinks for selenium oxyions. Although anaerobic dissimilatory selenate reduction was first demonstrated in two pure cultures [16], [20] only a few additional isolates have been described since. Thauera selenatis [17] and Sulfurospirillium barnesii [22] are the two best-characterized bacteria, isolated for their dissimilatory selenate reducing capability. In both of these strains, selenate reduction follows stoichiometric accumulation of selenite, although in the presence of nitrite, T. selenatis can reduce selenite to elemental selenium [5].

The isolation of extremophilic selenate-respiring microorganisms such as Pyrobaculum arsenaticum (an hyperthermophilic archeaon) [11], Selenihalanaerobacter shriftii (halophile) [3], Bacillus selenitireducens and B. arsenicoselenatis (both alkaliphiles) [2] and also a Bacillus strain SF1 [9] from an uncontaminated aquatic system has opened up new avenues for microbial ecologists. Most of the dissimilatory selenate reducing microbes use short chain fatty acids or H2 as electron donor. Here we describe a novel dissimilatory selenate reducing bacterium, strain AK4OH1, isolated from estuarine sediment, which uses 4-hydroxybenzoate as the carbon and energy source [12]. This coupling of an aromatic substrate with selenate respiration has not been described before. Strain AK4OH1 is a new member of the Gammaproteobacteria for which we propose the name Sedimenticola selenatireducens.

Section snippets

Bacterial isolates

Strains AK4OH1 and Ke4OH1 were previously isolated from sediment grab samples from the Arthur Kill, an inter-tidal region between Staten Island, NY-NJ and the Kesterson reservoir, CA respectively, after enrichment with Na2SeO4 as the terminal electron acceptor and 4-hydroxybenzoate as electron donor [12]. Strain AK4OH1 was maintained in anaerobic soft agar shake tubes where it forms bright red colonies from precipitation of elemental selenium. At this time we have been unable to revive strain

Morphology

Strain AK4OH1 is a rod shaped bacterium about 1.5 μm long. It is Gram-negative, strictly anaerobic, and non-motile. Phase contrast microscopy shows the accumulation of small refractile granules inside the cells (Fig. 1A). Transmission electron micrographs of selenate-grown cultures shows dark-electron dense granules believed to be elemental selenium deposited inside and outside of the cells (Fig. 1B and C). Upon prolonged exposure to the electron beam, these granules vaporize thus resulting in

Acknowledgements

This work was supported in part by the New Jersey Water Resource Research Institute. We are very thankful to Jonna Coombs for help with phylogenetic analysis and Heather Wiatrowski for help with DNA extraction protocols. We are grateful to Norberto Palleroni for photomicrographs, Valentin Starovoytov for electron micrographs and Norberto Palleroni and Hans G. Trüper for advice with the nomenclature.

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