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.
Highlights
A significant part of the Earth’s biosphere is exposed to regimes of extreme energy limitation, such as the terrestrial deep biosphere, the deep sea, and deep zones of most marine sediments
The vertically integrated areal fluxes of sulfide caused by sulfate reduction determined in all ten samples were highly variable. Their average (30.4 nmol S cm−2 d−1) was in the range of sulfide consumption by anoxygenic photosynthesis we found in the mats
Our results show that bacteria in the mats of magical blue hole (MBH) perform anoxygenic photosynthesis under extremely low light conditions
Summary
A significant part of the Earth’s biosphere is exposed to regimes of extreme energy limitation, such as the terrestrial deep biosphere, the deep sea, and deep zones of most marine sediments. The lower limits of biotic utilization of light are reached by anoxygenic photosynthesis, especially by members of the monophyletic clade of the GSB (Chlorobiaceae), which are obligate anaerobes and obligate anoxygenic phototrophs. They can proliferate at the interface of the sulfidic and photic zone in meromictic or eutrophic lakes (Montesinos et al, 1983; Mori et al, 2013; Crowe et al, 2014) or in microbial mats (Engel et al, 2004; Lau et al, 2009). Since the physical light attenuation of water is lowest between 400 and 500 nm (Sogandares and Fry, 1997), they are able to thrive at great water depths
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