Coupled reductive and oxidative sulfur cycling in the phototrophic plate of a meromictic lake

Abstract

Mahoney Lake represents an extreme meromictic model system and is a valuable site for examining the organisms and processes that sustain photic zone euxinia (PZE). A single population of purple sulfur bacteria (PSB) living in a dense phototrophic plate in the chemocline is responsible for most of the primary production in Mahoney Lake. Here, we present metagenomic data from this phototrophic plate--including the genome of the major PSB, as obtained from both a highly enriched culture and from the metagenomic data--as well as evidence for multiple other taxa that contribute to the oxidative sulfur cycle and to sulfate reduction. The planktonic PSB is a member of the Chromatiaceae, here renamed Thiohalocapsa sp. strain ML1. It produces the carotenoid okenone, yet its closest relatives are benthic PSB isolates, a finding that may complicate the use of okenone (okenane) as a biomarker for ancient PZE. Favorable thermodynamics for non-phototrophic sulfide oxidation and sulfate reduction reactions also occur in the plate, and a suite of organisms capable of oxidizing and reducing sulfur is apparent in the metagenome. Fluctuating supplies of both reduced carbon and reduced sulfur to the chemocline may partly account for the diversity of both autotrophic and heterotrophic species. Collectively, the data demonstrate the physiological potential for maintaining complex sulfur and carbon cycles in an anoxic water column, driven by the input of exogenous organic matter. This is consistent with suggestions that high levels of oxygenic primary production maintain episodes of PZE in Earth's history and that such communities should support a diversity of sulfur cycle reactions.

Contrasting taxonomic stratification of microbial communities in two hypersaline meromictic lakes

“…In spite of their different genesis, they belong to the same type of meromictic lakes, where the water column overturn is hampered by strong salinity gradients. Although studies investigating the microbiota and substance turnover in meromictic lakes are available (Biderre-Petit et al, 2011;Habicht et al, 2011;Hamilton et al, 2014), most of the ones concerning the hypersaline water bodies were performed on Arctic (Pouliot et al, 2009;Comeau et al, 2012) or Antarctic (Bowman et al, 2000;Lauro et al, 2011) lakes. Although information on temperate neutral hypersaline meromictic lakes microbiota are scarce, previous investigations on Ursu Lake prokaryotes (using community-level physiological profiling, culture-dependent and PCR-denaturing gradient gel electrophoresis methods) have shown the presence of active and diverse communities (Cristea et al, 2014;Máthé et al, 2014); yet, a detailed molecular diversity study is not available to date.…”

Spatially resolved capture of hydrogen sulfide from the water column and sedimentary pore waters for abundance and stable isotopic analysis

“…It is characterized by anoxic and sulfidic (euxinic) waters below a depth of approximately 7 m (Gilhooly et al, 2016). The shallowness of the chemocline means that the top of the sulfidic waters are in the photic zone, enabling a dense layer of photosynthetic purple sulfur bacteria to colonize the chemocline (e.g., Figure 5a) (Hamilton, 2014). As a result, sulfide is removed by both phototrophic sulfide oxidation as well as abiotic oxidation with oxygen (Overmann et al, 1996).…”

Testing the ancient marine redox record from oxygenic photosynthesis to photic zone euxina

“…carotenoid okenane Hamilton et al, 2014). According to observations of modern systems, planktonic Chromatiaceae that produce okenone grow in water columns where the oxic/anoxic boundary is <24 m and in most cases <12 m Hamilton et al, 2014).…”

“…According to observations of modern systems, planktonic Chromatiaceae that produce okenone grow in water columns where the oxic/anoxic boundary is <24 m and in most cases <12 m Hamilton et al, 2014). Okenane is a proposed marker of planktonic Chromatiaceae, but the potential contribution of okenane from mat---dwelling Chromatiaceae in the geologic record is currently debated (e.g.…”

“…Okenane is a proposed marker of planktonic Chromatiaceae, but the potential contribution of okenane from mat---dwelling Chromatiaceae in the geologic record is currently debated (e.g. Hamilton et al, 2014). Okenane was first reported in rock extracts from the Barney Creek Formation (BCF; 1.64 Ga) .…”