A New Microbial Player on the Iron Redox Court of Shallow-Water Hydrothermal Vents

Abstract:

The Fe(III)/Fe(II) couple is thought to have been a significant early energy metabolism involved in some of the first biogeochemical processes on Earth (Weber et al., 2006). The early evolving and metal-rich nature of modern hydrothermal systems remain particularly significant for Fe-based activities (Vargas et al., 1998). Documented evidence from such systems show a variety of yet unknown microbial lineages potentially linked to the history of Fe (i.e., Meyer-Dombard and Amend, 2014). Here we describe a novel microbe that reduces Fe(III) at shallow-water hydrothermal vents in Milos Island, Greece. Our laboratory experiments show this strain, MAG-PB1^T, to reduce Fe(III) between 30 - 70 °C, 0 - 50 g NaCl l^-1 and pH 5.5 - 8.0. Shortest generation time occurred under optimal conditions (60 °C, ~1.8 g NaCl l^-1, pH 6.0) with H₂ as the energy source, CO₂ as the carbon source and Fe(III) as electron acceptor. Its metabolic characteristics are, however, not limited to this pathway. Strain MAG-PB1^T can also reduce Mn(IV), arsenate and selenate. Its use of at least 9 organic substrates as energy or carbon sources also demonstrates its mixotrophy.

Phylogenetic 16S rRNA gene analyses place strain MAG-PB1^T within the Deltaproteobacteria, with the closest match (99%) being an uncultured microbe from hydrothermal springs in Ambitle Island, Papua New Guinea (Meyer-Dombard and Amend, 2014). Its next closest match (97%) is Deferrisoma camini, isolated from a deep-sea vent in the Eastern Lau Spreading Center (Slobodkina et al. 2012). Our strain represents a novel species, which we named Deferrisoma paleochoriense. The occurrence of D. paleochoriense in the shallow-water vents of Milos and Ambitle islands coincides with high arsenic, iron and sulfide contents (Akerman et al., 2011; Price et al., 2013; Yücel et al., 2013). Consequently, our study provides important physiological and metabolic evidence of the feedback between metal chemistry and life in hydrothermal sytems rich in iron and arsenic.