Community Shift from Phototrophic to Chemotrophic Sulfide Oxidation following Anoxic Holomixis in a Stratified Seawater Lake

Abstract

f Most stratified sulfidic holomictic lakes become oxygenated after annual turnover. In contrast, Lake Rogoznica, on the eastern Adriatic coast, has been observed to undergo a period of water column anoxia after water layer mixing and establishment of holomictic conditions. Although Lake Rogoznica's chemistry and hydrography have been studied extensively, it is unclear how the microbial communities typically inhabiting the oxic epilimnion and a sulfidic hypolimnion respond to such a drastic shift in redox conditions. We investigated the impact of anoxic holomixis on microbial diversity and microbially mediated sulfur cycling in Lake Rogoznica with an array of culture-independent microbiological methods. Our data suggest a tight coupling between the lake's chemistry and occurring microorganisms. During stratification, anoxygenic phototrophic sulfur bacteria were dominant at the chemocline and in the hypolimnion. After an anoxic mixing event, the anoxygenic phototrophic sulfur bacteria entirely disappeared, and the homogeneous, anoxic water column was dominated by a bloom of gammaproteobacterial sulfur oxidizers related to the GSO/SUP05 clade. This study is the first report of a community shift from phototrophic to chemotrophic sulfide oxidizers as a response to anoxic holomictic conditions in a seasonally stratified seawater lake. Stratified sulfidic lakes offer a physically and chemically welldefined environment for the development of complex yet stable microbial communities along light, oxygen, and sulfide gradients (1-4). Their water column is divided into an oxic surface layer, the epilimnion, and an anoxic bottom layer, the hypolimnion (5). The interface between these layers is the chemocline. It is the zone of highest chemical reactivity in the lake, typically accompanied by elevated microbial activity. In the anoxic hypolimnion and the underlying sediments, sulfate reduction plays a key role in organic matter remineralization (e.g., see references 3 and 6), resulting in the production of hydrogen sulfide. Where sulfide and light are present but oxygen is absent, anoxygenic phototrophic green sulfur bacteria (GSB) and purple sulfur bacteria (PSB) oxidize sulfide and form extensive blooms with cell densities of up to 10 7 cells ml Ϫ1 (1, 3, 7-10). Chemotrophic sulfur oxidizers (e.g., Alphaproteobacteria, Gammaproteobacteria, and Epsilonproteobacteria) often occur in layers above or together with GSB and PSB at the chemocline (3, 9, 11-13). In the oxic, sulfide-free epilimnion, the microbial community composition is distinct from those in underlying anoxic waters (10,13,14). Lake Rogoznica is a seasonally stratified seawater lake on the Croatian Adriatic coast. Its hydrography and chemistry have been studied extensively throughout the last 2 decades. The epilimnion is similar to waters of the adjacent Adriatic Sea in temperature and salinity, while the hypolimnion is highly enriched in nutrients (NH 4 ϩ , up to 150 M; PO 4 3Ϫ , up to 22 M; SiO 4 4Ϫ , up to 400 M) and dissolved organic carbon (DOC) (up to 6 mg...

High potential for temperate viruses to drive carbon cycling in chemoautotrophy‐dominated shallow‐water hydrothermal vents

“…To our knowledge, this represents the first experimental evidence of the potentially high functional impact of temperate viruses on natural microbial assemblages in chemoautotrophs‐dominated marine ecosystems (Howard‐Varona et al ., ). As epsilonproteobacteria, including the Sulfurovum gen ., can be abundant also in non‐vent environments (Pjevac et al ., ; ; Hamilton et al ., ), our results trigger future research on the possibly relevant role of similar provirus‐host dynamics also in other ecosystems.…”

Microbial Surface Colonization and Biofilm Development in Marine Environments

“…Some MRC bacteria synthesize and store poly-␤-hydroxyalkanoates when carbon and energy resources are available but inorganic nutrients are limiting (781,782), which may enhance bacterial viability via poly-␤-hydroxyalkanoate catabolism when other sources of organic substrates are scarce (594). Some MRC bacteria also carry out lithotrophic sulfur oxidation to conserve additional energy (783,784), which may be explored to enhance anaplerotic CO 2 fixation, growth, and survival (761,785). These traits provide MRC bacteria with additional competitive advantages for energy acquisition, energy conservation, and stabilization of bacterium-alga and bacteriumsurface associations.…”

In situ abundance and carbon fixation activity of distinct anoxygenic phototrophs in the stratified seawater lake Rogoznica

“…The recorded chemical and hydrographical water profiles were in accordance with data collected on numerous occasions in spring time over the last three decades (e.g. Bura‐Nakić et al ., ; Pjevac et al ., ). The salinity of the deeper water layers was similar to the surrounding Adriatic seawater source (Lipizer et al ., ).…”

“…Interestingly, even above the anoxic chemocline (at 8 m), BChl e concentrations (0.5 nmol l −1 ) exceeded BChl a concentrations (0.1 nmol l −1 ). Since BChl e is only found in GSB, while BChl a is present in a variety of anoxygenic phototrophic bacteria, the BChl e /BChl a ratio supports the previously reported dominance of GSB throughout the chemocline of Lake Rogoznica (Pjevac et al ., ).…”