Low-light anoxygenic photosynthesis and Fe-S-biogeochemistry in a microbial mat

Sebastian Haas, Dirk de Beer, Judith M. Klatt, Artur Fink, Rebecca Mc Cauley Rench, Trinity L. Hamilton, Volker Meyer, Brian Kakuk, Jennifer L. Macalady

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6 Scopus citations

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.

Original languageEnglish (US)
Article number858
JournalFrontiers in Microbiology
Volume9
Issue numberAPR
DOIs
StatePublished - Apr 27 2018

Bibliographical note

Funding Information:
We are indebted to J?rg Overmann and his group at DSMZ Braunschweig for providing freeze-dried Chlorobium culture material. We thank Marit van Erk for the S0 analyses, Arjun Chennu, Tim Ferdelman, Mohammad al-Najjar, and Gaute Lavik for the expert advice on methodology, as well as Martina Alisch, Gabriele Klockgether, and all MPI Microsensor TAs for helping with sample analysis and microsensor preparation. Furthermore, we thank Tomas Wilkop and Manfred Schl?sser for their support in preparing the field excursion, and the MPI Electronics and Mechanics workshops for their technical ingenuity. Sean Crowe provided valuable inspiration for Proterozoic Ocean implications. Three anonymous reviewers from an unsuccessful previous submission of the manuscript gave valuable suggestions for improvement. SH feels indebted to the Max-Planck society and the MarMic program for the excellent scientific training and funding. This study was funded by the Max-Planck Institute for Marine Microbiology, the National Science Foundation (EAR-0525503 to JM), the NASA Astrobiology Institute (PSARC, NNA04CC06A to JM), a Lewis and Clark Fund for Exploration and Field Research in Astrobiology Fellowship (to RM), a National Science Foundation Graduate Research Fellowship Travel Grant (to RM), the Canadian Excellence Research Chair in Oceanography (SH), and the NASA Astrobiology Institute Postdoctoral Program (TH)

Keywords

  • Anoxygenic photosynthesis
  • Bacteriochlorophyll e
  • Green sulfur bacteria
  • Iron-sulfur-cycling
  • Low-light photosynthesis
  • Microbial mat
  • Proterozoic ocean
  • Sulfide scavenging

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