Characterization of the physiology and cell–mineral interactions of the marine anoxygenic phototrophic Fe(II) oxidizer Rhodovulum iodosum – implications for Precambrian Fe(II) oxidation

• Published in: FEMS microbiology ecology 2014-06, Vol.88 (3), p.503-515
• Main Authors: Wu, Wenfang, Swanner, Elizabeth D., Hao, Likai, Zeitvogel, Fabian, Obst, Martin, Pan, Yongxin, Kappler, Andreas
• Format: Article
• Language: English
• Subjects: anoxygenic phototrophic Fe(II) oxidation; banded iron formations; Ecology; Ferric Compounds - metabolism; Ferrous Compounds - metabolism; Fresh Water; Iron; Iron Compounds - chemistry; Light intensity; marine photoferrotroph; Microbiology; Microorganisms; Minerals; Minerals - chemistry; Oxidation; Oxidation-Reduction; Phototrophic Processes; Physiology; Precambrian; Rhodovulum - growth & development; Rhodovulum - metabolism; Rhodovulum - radiation effects; Rhodovulum iodosum; Seawater; Seawater - chemistry
• ISSN: 0168-6496; 1574-6941
• DOI: 10.1111/1574-6941.12315

Abstract Anoxygenic phototrophic Fe(II)-oxidizing bacteria (photoferrotrophs) are suggested to have contributed to the deposition of banded iron formations (BIFs) from oxygen-poor seawater. However, most studies evaluating the contribution of photoferrotrophs to Precambrian Fe(II) oxidation have used freshwater and not marine strains. Therefore, we investigated the physiology and mineral products of Fe(II) oxidation by the marine photoferrotroph Rhodovulum iodosum. Poorly crystalline Fe(III) minerals formed initially and transformed to more crystalline goethite over time. During Fe(II) oxidation, cell surfaces were largely free of minerals. Instead, the minerals were co-localized with EPS suggesting that EPS plays a critical role in preventing cell encrustation, likely by binding Fe(III) and directing precipitation away from cell surfaces. Fe(II) oxidation rates increased with increasing initial Fe(II) concentration (0.43–4.07 mM) under a light intensity of 12 μmol quanta m−2s−1. Rates also increased as light intensity increased (from 3 to 20 μmol quanta m−2s−1), while the addition of Si did not significantly change Fe(II) oxidation rates. These results elaborate on how the physical and chemical conditions present in the Precambrian ocean controlled the activity of marine photoferrotrophs and confirm the possibility that such microorganisms could have oxidized Fe(II), generating the primary Fe(III) minerals that were then deposited to some Precambrian BIFs. This study confirms the possibility that marine photoferrotrophs could have deposited Precambrian BIFs and highlights the physical and chemical factors controlling their physiology and activity. This paper examines the physiology of the marine anoxygenic phototrophic Fe(II) oxidizer, Rhodovulum iodosum, as a model for evaluating the contribution of photoferrotrophs to Precambrian Fe(II) oxidation. Photoferrotrophs were likely important contributors to the biogeochemistry of Precambrian oceans, and as such figure prominently in the co-evolution of microbial life and Earth surface chemistry.