Iron encrustations on filamentous algae colonized by <i>Gallionella</i>-related bacteria in a metal-polluted freshwater stream

Abstract

Abstract. Filamentous macroscopic algae were observed in slightly acidic to circumneutral (pH 5.9~6.5) metal-rich stream water that leaked out in a former uranium-mining district (Ronneburg, Germany). These algae differ in color and morphology and were encrusted with Fe-deposits. To elucidate the potential interaction with Fe(II)-oxidizing bacteria (FeOB), we collected algal samples at three time points during summer 2013 and studied the algae-bacteria-mineral compositions via confocal laser scanning microscopy (CLSM), scanning electronic microscopy, Fourier transform infrared spectra, and a 16S and 18S rRNA gene based bacterial and algae community analysis. Surprisingly, sequencing analysis of 18S rRNA gene regions of green and brown algae revealed high homologies with the yellow-green freshwater algae Tribonema (99.9~100%). CLSM imaging indicates a loss of active chloroplasts in the algae cells, which may be responsible for the change in color in Tribonema. Fe(III)-precipitates on algal cells identified as ferrihydrite and schwertmannite were associated with microbes and extracellular polymeric substances (EPS)-like glycoconjugates. While the green algae were fully encrusted with Fe-precipitates, the brown algae often exhibited discontinuous series of precipitates. This pattern was likely due to the intercalary growth of algal filaments which allowed them to avoid fatal encrustation. 16S rRNA gene targeted studies based on DNA and RNA revealed that Gallionella-related FeOB dominated the bacterial RNA and DNA communities (70–97 and 63–96%, respectively) suggesting their contribution to Fe(II) oxidation. Quantitative PCR revealed higher Gallionella-related 16S rRNA gene copy numbers on the surface of green algae compared to the brown algae. The latter harbored a higher microbial diversity, including some putative predators of algae. Lower photosynthetic activities of the brown algae lead to reduced EPS production which may have enabled predator colonization. The differences observed between green and brown algae suggest that metal-tolerant Tribonema sp. provide suitable microenvironments for microaerophilic Fe-oxidizing bacteria. However, high levels of iron orchres can be fatal to the alga.