Respiratory succession and community succession of bacterioplankton in seasonally anoxic estuarine waters

Anoxia occurs in bottom waters of stratified estuaries when respiratory consumption of oxygen, primarily by bacteria, outpaces atmospheric and photosynthetic reoxygenation. Once water becomes anoxic, bacterioplankton must change their metabolism to some form of anaerobic respiration. Analysis of redox chemistry in water samples spanning the oxycline of Chesapeake Bay during the summer of 2004 suggested that there was a succession of respiratory metabolism following the loss of oxygen. Bacterial community doubling time, calculated from bacterial abundance (direct counts) and production (anaerobic leucine incorporation), ranged from 0.36 to 0.75 day and was always much shorter than estimates of the time that the bottom water was anoxic (18 to 44 days), indicating that there was adequate time for bacterial community composition to shift in response to changing redox conditions. However, community composition (as determined by PCR-denaturing gradient gel electrophoresis analysis of 16S rRNA genes) in anoxic waters was very similar to that in surface waters in June when nitrate respiration was apparent in the water column and only partially shifted away from the composition of the surface community after nitrate was depleted. Anoxic water communities did not change dramatically until August, when sulfate respiration appeared to dominate. Surface water populations that remained dominant in anoxic waters were Synechococcus sp., Gammaproteobacteria in the SAR86 clade, and Alphaproteobacteria relatives of Pelagibacter ubique, including a putative estuarine-specific Pelagibacter cluster. Populations that developed in anoxic water were most similar (<92% similarity) to uncultivated Firmicutes, uncultivated Bacteroidetes, Gammaproteobacteria in the genus Thioalealovibrio, and the uncultivated SAR406 cluster. These results indicate that typical estuarine bacterioplankton switch to anaerobic metabolism under anoxic conditions but are ultimately replaced by different organisms under sulfidic conditions.