Deep-water anoxygenic photosythesis in a ferruginous chemocline S. A. CROWE, 1,2 J. A. MARESCA, 3,4 C. JONES, 1,2 A. STURM, 5 C. HENNY, 6 D. A. FOWLE, 5 R. P. COX, 7 E. F. DELONG 3 AND D. E. CANFIELD 1 1 Nordic Center for Earth Evolution and Institute of Biology, University of Southern Denmark, Odense, Denmark 2 Departments of Microbiology & Immunology and Earth, Ocean, & Atmospheric Sciences, University of British Columbia, Vancouver, Canada 3 Department of Civil and Environmental Engineering, MIT, Cambridge, MA, USA 4 Depatment of Civil and Environmental Engineering, University of Delaware, Newark, DE, USA 5 Department of Geology, University of Kansas, Lawrence, KS, USA 6 Limnology Division, Indonesian Institute of Sciences, Cibinong, Indonesia 7 Nordic Center for Earth Evolution and Department of Biochemistry and Molecular Biology, University of Southern Denmark, Odense, Denmark ABSTRACT Ferruginous Lake Matano, Indonesia hosts one of the deepest anoxygenic photosynthetic communities on Earth. This community is dominated by low-light adapted, BChl e-synthesizing green sulfur bacteria (GSB), which comprise ~25% of the microbial community immediately below the oxic-anoxic boundary (OAB; 115-120 m in 2010). The size of this community is dependent on the mixing regime within the lake and the depth of the OAB—at ~117 m, the GSB live near their low-light limit. Slow growth and C-fixation rates suggest that the Lake Matano GSB can be supported by sulfide even though it only accumulates to scarcely detectable (low lM to nM) concentrations. A model laboratory strain (Chlorobaculum tepidum) is indeed able to access HS  for oxidation at nM concentrations. Furthermore, the GSB in Lake Matano possess a full complement of S-oxidizing genes. Together, this physiological and genetic information suggests that deep- water GSB can be supported by a S-cycle, even under ferruginous conditions. The constraints we place on the metabolic capacity and physiology of GSB have important geobiological implications. Biomarkers diag- nostic of GSB would be a good proxy for anoxic conditions but could not discriminate between euxinic and ferruginous states, and though GSB biomarkers could indicate a substantial GSB community, such a com- munity may exist with very little metabolic activity. The light requirements of GSB indicate that at light lev- els comparable to those in the OAB of Lake Matano or the Black Sea, GSB would have contributed little to global ocean primary production, nutrient cycling, and banded iron formation (BIF) deposition in the Pre- cambrian. Before the proliferation of oxygenic photosynthesis, shallower OABs and lower light absorption in the ocean’s surface waters would have permitted greater light availability to GSB, potentially leading to a greater role for GSB in global biogeochemical cycles. Received 3 December 2013; accepted 8 April 2014 Corresponding author: S. A. Crowe. Tel.: +1 604 827 3827; fax: +1 604 822 6041; e-mail: sean.crowe@ubc.ca INTRODUCTION Ferruginous conditions (anoxic and Fe-rich) have domi- nated ocean chemistry throughout much of Earth’s history (Canfield et al., 2008; Planavsky et al., 2011; Poulton & Canfield, 2011). The ecology of these ferruginous oceans is the subject of much debate and speculation (Canfield et al., 2006), as organisms inhabiting such Fe-centric eco- systems likely played a pivotal role in shaping the chemistry of the modern Earth (Canfield et al., 2006; Poulton & Canfield, 2011). Of particular contention are the roles that anoxygenic phototrophs may have played in early Earth primary production (Garrels & Perry, 1974; Canfield et al., 2006), the deposition of banded iron formations (BIFs) 322 © 2014 John Wiley & Sons Ltd Geobiology (2014), 12, 322–339 DOI: 10.1111/gbi.12089