A Study on Microbial Ecology in Permanently Ice-covered Lakes of McMurdo Dry Valleys, Antarctica

Abstract

Antarctica has been considered as pristine and harsh environment in respect to microbes because of the extreme conditions. Perennially ice-covered lakes (Lake Fryxell, Lake Miers, and Lake Bonney) in the McMurdo Dry Valleys, Antarctica, are chemically stratified with depth and have distinct biological gradients. Despite of long-term research on these unique environments, the information on the structure of the microbial communities in the water columns of these lakes are scarce. In this study, bacterial diversity in the ice-covered lakes in Antarctica was examined by 16S rRNA gene-based pyrosequencing. Distinct communities were present in each lake, reflecting the unique biogeochemical characteristics of these environments. Further, certain bacterial lineages were exclusively confined to specific depths within each lake. For example, candidate division WM88 occurred solely at a depth of 15 m in Lake Fryxell, whereas unknown lineages of Chlorobi were found only at a depth of 18 m in Lake Miers, and two distinct classes of Firmicutes inhabited East and West Lobe Bonney at depth of 30 m. Redundancy analysis revealed that community variation of bacterioplankton could be explained by the distinct conditions of each lake and depth

in particular, assemblages from layers beneath the chemocline had biogeochemical associations that differed from those in the upper layers. Despite of the fact that sulfate reduction has been actively detected, little is known about diversity of sulfate reducing bacteria in Lake Fryxell. Less than 1% of total bacteria are known to be culturable. By application of culture-independent approach such as metagenomics, not only full extent of bacterial diversity but also their ecological function could be obtained. Three draft genomes were recovered from metagenome data as sulfate reduction-related bacteria, two belonging to Deltaproteobacteria and one belonging to candidate division WM88. Deltaproteobacteria was a key player for sulfate reduction in Lake Fryxell whereas candidate division WM88 was indirectly related to the reaction of sulfate reduction. Other metabolic pathways were also investigated, and it was revealed that they were versatile in acquisition and usage of various carbon sources and energy conservation. Another aspect of sulfate reducing bacteria in the bottom of Lake Fryxell was observed based on microcosm study as a culture-dependent approach. Through performing microcosm study using the lake water as a medium, previously uncultivated sulfate reducing bacteria were expected to be recovered from Lake Fryxell. From the microcosm culture, the genus Desulfosporosinus belonging to the phylum Firmicutes was surprisingly enriched in large proportion under specific conditions with low concentration of carbon source and sulfate. This genus has gained attention for the ability of sulfate reduction with high efficiency albeit low abundance in natural environments, which is known as rare biosphere. The findings of patterns of bacterial community composition and their ecological functions, including sulfate reduction, may represent adaptation of bacteria to the extreme and unique biogeochemical gradients of ice-covered lakes in the McMurdo Dry Valleys. Also, novel results may provide further insights into the ecology and evolution of bacteria inhabiting the ice-covered lakes of Antarctica.