Low-Light Anoxygenic Photosynthesis and Fe-S-Biogeochemistry in a Microbial Mat

Sebastian Haas; Dirk de Beer; Judith M Klatt; Artur Fink; Rebecca McCauley Rench; Trinity L Hamilton; Volker Meyer; Brian Kakuk; Jennifer L Macalady

doi:10.3389/fmicb.2018.00858

Low-Light Anoxygenic Photosynthesis and Fe-S-Biogeochemistry in a Microbial Mat

Front Microbiol. 2018 Apr 27:9:858. doi: 10.3389/fmicb.2018.00858. eCollection 2018.

Authors

Sebastian Haas^{1

2}, Dirk de Beer¹, Judith M Klatt^{1

3}, Artur Fink¹, Rebecca McCauley Rench⁴, Trinity L Hamilton⁵, Volker Meyer¹, Brian Kakuk⁶, Jennifer L Macalady⁴

Affiliations

¹ Max Planck Institute for Marine Microbiology, Bremen, Germany.
² Department of Oceanography, Dalhousie University, Halifax, NS, Canada.
³ Department of Earth and Environmental Sciences, University of Michigan, Ann Arbor, MI, United States.
⁴ Geosciences Department, Pennsylvania State University, University Park, PA, United States.
⁵ Department of Plant and Microbial Biology, University of Minnesota, Minneapolis, MN, United States.
⁶ Bahamas Caves Research Foundation, Marsh Harbour, Bahamas.

Abstract

We report extremely low-light-adapted anoxygenic photosynthesis in a thick microbial mat in Magical Blue Hole, Abaco Island, The Bahamas. Sulfur cycling was reduced by iron oxides and organic carbon limitation. The mat grows below the halocline/oxycline at 30 m depth on the walls of the flooded sinkhole. In situ irradiance at the mat surface on a sunny December day was between 0.021 and 0.084 μmol photons m^-2 s^-1, and UV light (<400 nm) was the most abundant part of the spectrum followed by green wavelengths (475-530 nm). We measured a light-dependent carbon uptake rate of 14.5 nmol C cm^-2 d^-1. A 16S rRNA clone library of the green surface mat layer was dominated (74%) by a cluster (>97% sequence identity) of clones affiliated with Prosthecochloris, a genus within the green sulfur bacteria (GSB), which are obligate anoxygenic phototrophs. Typical photopigments of brown-colored GSB, bacteriochlorophyll e and (β-)isorenieratene, were abundant in mat samples and their absorption properties are well-adapted to harvest light in the available green and possibly even UV-A spectra. Sulfide from the water column (3-6 μmol L^-1) was the main source of sulfide to the mat as sulfate reduction rates in the mats were very low (undetectable-99.2 nmol cm^-3 d^-1). The anoxic water column was oligotrophic and low in dissolved organic carbon (175-228 μmol L^-1). High concentrations of pyrite (FeS₂; 1-47 μmol cm^-3) together with low microbial process rates (sulfate reduction, CO₂ fixation) indicate that the mats function as net sulfide sinks mainly by abiotic processes. We suggest that abundant Fe(III) (4.3-22.2 μmol cm^-3) is the major source of oxidizing power in the mat, and that abiotic Fe-S-reactions play the main role in pyrite formation. Limitation of sulfate reduction by low organic carbon availability along with the presence of abundant sulfide-scavenging iron oxides considerably slowed down sulfur cycling in these mats.

Keywords: Proterozoic ocean; anoxygenic photosynthesis; bacteriochlorophyll e; green sulfur bacteria; iron-sulfur-cycling; low-light photosynthesis; microbial mat; sulfide scavenging.