Remarkable Diversity of Phototrophic Purple Bacteria in a Permanently Frozen Antarctic Lake

Abstract

Although anoxygenic photosynthesis is thought to play an important role in the primary productivity of permanently frozen lakes in the Antarctic dry valleys, the bacterial communities responsible for this metabolism remain uncharacterized. Here we report the composition and activity of phototrophic purple bacteria in Lake Fryxell, Antarctica, as determined by analysis of a photosynthesis-specific gene, pufM. The results revealed an extensive diversity and highly stratified distribution of purple nonsulfur bacteria in Lake Fryxell and showed which phylotypes produced pufM transcripts in situ. Enrichment cultures for purple bacteria yielded two morphotypes, each with a pufM signature identical to signatures detected by environmental screening. The isolates also contained gas vesicles, buoyancy structures previously unknown in purple nonsulfur bacteria, that may be necessary for these organisms to position themselves at specific depths within the nearly freezing water column.Lake Fryxell is a meromictic lake located 18 m above sea level at the entrance of Taylor Valley adjacent to McMurdo Sound, Antarctica (17). The lake is a closed basin with a maximum depth of 19 m (28). Lake Fryxell has undergone several dry-down periods in the past, resulting in slightly saline bottom waters overlaid with more dilute water introduced from glacial meltwater streams (12,20). This process has resulted in a gradient of solutes in the water column that is further stabilized by a perennial ice cover that is 3 to 5 m thick (25,28). The mixolimnion of the water column is supersaturated with oxygen, while the monimolimnion is anoxic due to limited gas exchange imposed by the perennial ice cover. The latter also serves as a barrier to light penetration, allowing only a small amount of light to reach the water column; for example, in Lake Fryxell, photosynthetically active radiation (PAR) is reduced by more than 90% from a depth of 4 to 9 m and by another 90% from 9 to 11 m (2, 23).There have been extensive studies of the geochemistry of Lake Fryxell, but to date only a few studies of the microbial communities that inhabit the lake have been reported (16,24). These studies focused on ammonia-oxidizing bacteria (members of the ␥ and ␤ subdivisions of the Proteobacteria) within the water column and the contributions of cyanobacteria inhabiting the lake's ice cover to primary production in the dry valley ecosystem (6, 29). Studies of the bacterial diversity of microbial mat samples collected from moats that surround the lake during the austral summer season showed a large degree of microbial diversity, including both gram-positive and gramnegative bacteria, as well as Archaea (4).The presence of a year-round ice layer on Lake Fryxell prevents active mixing and maintains an extensive anoxic zone containing sulfide, which is suitable for development of anoxygenic phototrophic purple bacteria (21, 23). These organisms, although phototrophic, do not evolve oxygen and are members of the ␣, ␤, and ␥ subdivisions of the Proteobacteria (10, 11). The...

Diversity and abundance of aerobic anoxygenic phototrophic bacteria in two cyanobacterial bloom-forming lakes in China

“…This was different from the previous reports that found Betaproteobacterial AAP bacteria to be the predominant bacteria in freshwater bodies (Karr et al, 2003;Kirchman, 2005, 2008). The distribution of AAP bacteria can be influenced by various factors, such as light, UV, water chemistry, salinity, chlorophyll a, and particles (Jiao et al, 2007; Table 1.…”

“…Phylogenetic analysis based on pufM and other photosynthesis genes suggests that Alphaproteobacterial and Gammaproteobacterial AAP bacteria are abundant in oceans and saline lakes, whereas Betaproteobacteria are predominant in freshwater bodies (Yurkova et al, 2002;Allgaier et al, 2003;Karr et al, 2003;Waidner and Kirchman, 2005Jiang et al, 2009). The discovery of AAP bacteria in open seas suggests that AAP bacteria can adapt to oligotrophic waters because light might provide supplementary energy in low-nutrient conditions (Kolber et al, 2000(Kolber et al, , 2001.…”

Ace Lake: three decades of research on a meromictic, Antarctic lake

“…While we are beginning to gain an idea through molecular analysis of the taxonomy of the communities of Bacteria and Archaea that live in the anoxic monimolimnion waters, we still have very little information on processes that drive the sulphur and methane cycles, or their magnitude. An approach that combines molecular and biogeochemical investigations is beginning to shed light on these important processes in the Lake Fryxell in the Dry Valleys (Karr et al 2003(Karr et al , 2006.…”

Roseobacter -Like Bacteria in Red and Mediterranean Sea Aerobic Anoxygenic Photosynthetic Populations

“…Recently, pufM genes were used to assess the remarkable diversity of different aerobic (7) and anaerobic (1,14) anoxygenic photosynthetic assemblages. Proteins in the bacteriochlorophyll biosynthetic pathway were also recently used as phylogenetic markers for different anoxygenic phototrophs (7).…”