Bacterial control of silicon regeneration from diatom detritus: Significance of bacterial ectohydrolases and species identity

Abstract

Bacteria (and possibly archaea) accelerate silica dissolution in the sea by colonizing and enzymatically degrading the organic matrix of diatom frustules. We tested whether colonizer species composition and ectohydrolase profiles critically control silicon regeneration by allowing diatom (Thalassiosira weissflogii and Chaetoceros simplex) detritus to be colonized by natural bacterial assemblages and 12 phylogenetically characterized marine isolates. We characterized the colonizers' ectohydrolase profiles and rates of silicon regeneration. The colonizers' cell‐specific protease activity was consistently the dominant ectohydrolase, and it strongly correlated with silica dissolution rates. Cell‐specific glucosidase, lipase, and chitinase activities showed no correlation with silicon regeneration. Denaturing gradient gel electrophoresis (DGGE) of PCR‐amplified 16S rRNA genes was used to monitor colonization of detritus by natural microbial assemblages and to identify colonizing phylotypes. Representatives from gammaproteobacteria and sphingobacteria‐flavobacteria classes dominated colonizer populations by comprising 65% and 25% of detected phylotypes, respectively. Archaea were not detected among colonizer populations. All bacterial isolates accelerated silica dissolution, but individual rates varied by >300%. Significant variability was observed within the Alteromonadaceae, which indicates different abilities to process diatom organic matter. Isolates that displayed enhanced colonization and protease activities were the most effective at regenerating silicon. The most effective isolate belonged to the sphingobacteria‐flavobacteria, a group specialized in colonizing marine particles. Other effective isolates grouped with Pseudoalteromonas, Alteromonas, and Vibrio genera. One isolate caused intense aggregation of diatom detritus, significantly reducing silicon regeneration. Our results indicate that bacterial species identity strongly controlled silicon regeneration by influencing the colonization potential and ectohydrolytic profiles of bacteria as well as aggregate formation. Mechanistic models of oceanic silica cycling should incorporate species composition and ectohydrolase profiles of bacteria involved in silicon regeneration.