Anaerobic respiration on tellurate and other metalloids in bacteria from hydrothermal vent fields in the eastern Pacific Ocean

Abstract

This paper reports the discovery of anaerobic respiration on tellurate by bacteria isolated from deep ocean (1,543 to 1,791 m) hydrothermal vent worms. The first evidence for selenite- and vanadate-respiring bacteria from deep ocean hydrothermal vents is also presented. Enumeration of the anaerobic metal(loid)-resistant microbial community associated with hydrothermal vent animals indicates that a greater proportion of the bacterial community associated with certain vent fauna resists and reduces metal(loid)s anaerobically than aerobically, suggesting that anaerobic metal(loid) respiration might be an important process in bacteria that are symbiotic with vent fauna. Isolates from Axial Volcano and Explorer Ridge were tested for their ability to reduce tellurate, selenite, metavanadate, or orthovanadate in the absence of alternate electron acceptors. In the presence of metal(loid)s, strains showed an ability to grow and produce ATP, whereas in the absence of metal(loid)s, no growth or ATP production was observed. The protonophore carbonyl cyanide m-chlorophenylhydrazone depressed metal(loid) reduction. Anaerobic tellurate respiration will be a significant component in describing biogeochemical cycling of Te at hydrothermal vents.

FIG. 1.

Percent resistance of cultivable aerobic and anaerobic epibiotic bacterial communities to Na₂SeO₃ (1,000 μg/ml), K₂TeO₃ (300 μg/ml), K₂TeO₄ (300 μg/ml), NaVO₃ (900 μg/ml), and Na₃VO₄ (1,000 μg/ml). Samples were from sulfide worms (A) and tubeworms (B). All populations were normalized to the highest CFU value measured for each animal and oxygenation treatment, which was assumed to represent 100% of the bacterial population under those conditions. Values provided are the means calculated from three samples each.

FIG. 2.

Metal(loid) reduction and morphology of deep ocean bacteria. (A) Anaerobic cultures of strains respiring metal(loid)s. −, cell-free control containing the metal(loid); +, cultures containing the indicated metal(loid). For metavanadate, the black and the rust-colored cultures contained 0.3 and 2 g/liter organics, respectively. For orthovanadate, the blue and the black cultures contained 0.7 and 2.2 g/liter organics, respectively. (B to E) Phase-contrast microscopy of anaerobic metal(loid)-amended ER-Se-17L, ER-Te-48, ER-V-6, and AV-V-25, respectively.

FIG. 3.

Anaerobic respiratory growth kinetics. (A) ER-Te-48 with various organics, with and without tellurate. (B) ER-V-6 with and without metavanadate. (C) AV-V-25 with and without orthovanadate. Metal(loid) concentrations are as described for Fig. 1.

FIG. 4.

Intracellular ATP concentrations. (A) ER-Te-48 with and without tellurate. (B) ER-V-6 with and without metavanadate.