A New Chemolithoautotrophic Arsenite-Oxidizing Bacterium Isolated from a Gold Mine: Phylogenetic, Physiological, and Preliminary Biochemical Studies

Abstract

A previously unknown chemolithoautotrophic arsenite-oxidizing bacterium has been isolated from a gold mine in the Northern Territory of Australia. The organism, designated NT-26, was found to be a gram-negative motile rod with two subterminal flagella. In a minimal medium containing only arsenite as the electron donor (5 mM), oxygen as the electron acceptor, and carbon dioxide-bicarbonate as the carbon source, the doubling time for chemolithoautotrophic growth was 7.6 h. Arsenite oxidation was found to be catalyzed by a periplasmic arsenite oxidase (optimum pH, 5.5). Based upon 16S rDNA phylogenetic sequence analysis, NT-26 belongs to the Agrobacterium/Rhizobium branch of the ␣-Proteobacteria and may represent a new species. This recently discovered organism is the most rapidly growing chemolithoautotrophic arsenite oxidizer known.Arsenic is found in many environments and is toxic to life in some forms. When present in insoluble forms, which are nontoxic, arsenic is frequently found as a mineral in combination with sulfur (e.g., orpiment [As 2 S 3 ] and realgar [AsS]) and especially with iron and sulfur (e.g., arsenopyrite [FeAsS]). The oxidation of these insoluble forms, chemically and/or microbiologically, results in the formation of arsenite (As III [H 3 AsO 3 ]). In environments such as acid mine drainage, arsenite concentrations can be extremely high (2 to 13 mg/liter) (22). The arsenite formed in various environments can then be oxidized to arsenate (As V [H 2 AsO 4 Ϫ ϩ H ϩ ]). Both of these soluble forms of arsenic, arsenite and arsenate, are toxic to living organisms, with arsenite considered more toxic than arsenate (5, 22).Interestingly, the chemical oxidation of arsenite to arsenate is slow. Most arsenite is, therefore, oxidized to arsenate microbiologically (22). Arsenite-oxidizing bacteria were first described in 1918 (7). These organisms, as well as a number of others that have been isolated more recently, are almost all heterotrophic arsenite-oxidizing bacteria, as they require the presence of organic matter for growth (17,18,23,24). The most common organism found has been Alcaligenes faecalis (7,17,18,23,24). For these heterotrophic bacteria, the oxidation (equation 1) is considered a detoxification mechanism rather than one that can support growth, despite the fact that the reaction is exergonic.Only one bacterium has been described that is able to use the energy gained from this reaction for growth. This organism, Pseudomonas arsenitoxidans, was found to grow chemolithoautotrophically with arsenite, oxygen, and carbon dioxide. The fastest doubling time reported for growth with arsenite was, however, in the order of 2 days (8). This report describes a new bacterium, isolated from a gold mine in the Northern Territory of Australia, that can also grow chemolithoautotrophically with arsenite as the electron donor, oxygen as the electron acceptor, and carbon dioxide (CO 2 ) or bicarbonate (HCO 3 Ϫ ) as the carbon source. Growth was rapid, with a doubling time of 7.6 h for chemolithoautotrophic grow...

Effect of soil microorganisms on arsenite oxidation in paddy soils under oxic conditions

“…Although Mnoxides are effective oxidants, the rate of As(III) oxidation decreases with time due to blocking of surface reactive sites by reaction products such as As(V), Mn(II) and possibly Mn(III) (Lafferty et al 2010a(Lafferty et al , 2010b. On the other hand, a large number of As(III)-oxidizing bacteria have been isolated from soils (Phillips and Taylor 1976;Santini et al 2000). They involve heterotrophic or autotrophic As(III) oxidizers, but it is not clear if such bacteria play significant role in As(III)-oxidizing processes in these environments.…”

Involvement of RpoN in Regulating Bacterial Arsenite Oxidation

“…Subsequent progress has been sporadic, with work that identified some organisms capable of As III oxidation (46,48,60) and then a study of a Pseudomonas arsenitoxidans strain reported to grow chemolithoautotrophically with As III as a sole electron donor (23). Subsequent follow-up characterizations of this organism and this process failed to materialize; however, approximately 2 decades later, Santini et al (52) described the isolation and initial characterization of a Rhizobiumlike bacterium (strain NT-26) that could grow chemolithoautotrophically with As III as a sole electron donor for energy generation and with CO 2 as a sole carbon source. Soon thereafter, and in part stimulated by the massive arsenic poisoning disaster in Bangladesh (2), a series of studies initiated the characterization of microbial As III oxidation in natural environments, including geothermal springs (9,11,12,17,19,24,25,35,51) and soils (41); in mining-contaminated environments (6,13,40); and, most recently, in anoxic photosynthesis (21,33 (28,31) indicated the role and importance of the sensor kinase AioS and its putative regulatory partner AioR (a bacterial enhancer binding protein), direct proof of these two proteins working together as part of a putative As III signal perception and transduction cascade was just recently provided by Sardiwal et al (54), who demonstrated the autophosphorylation of an AioS component and the AioS-specific phosphorylation of AioR.…”

Herminiimonas arsenicoxydans sp. nov., a metalloresistant bacterium

“…Physiologically diverse, these micro-organisms include both heterotrophic arsenite oxidizers and chemolithoautotrophic arsenite oxidizers (Santini et al, 2000;Oremland & Stolz, 2003;Silver & Phung, 2005). Heterotrophic oxidation of As [III] is viewed primarily as a detoxification reaction that converts As[III] encountered on the outer membrane of the cell into the less toxic and less mobile form As[V], perhaps making it less likely to enter the cell (Anderson et al, 1992).…”