Common Presence of Phototrophic <i>Gemmatimonadota</i> in Temperate Freshwater Lakes

Abstract

Members of the bacterial phylum <i>Gemmatimonadota</i> are ubiquitous in most natural environments and represent one of the top 10 most abundant bacterial phyla in soil. Sequences affiliated with <i>Gemmatimonadota</i> were also reported from diverse aquatic habitats; however, it remains unknown whether they are native organisms or represent bacteria passively transported from sediment or soil. To address this question, we analyzed metagenomes constructed from five freshwater lakes in central Europe. Based on the 16S rRNA gene frequency, <i>Gemmatimonadota</i> represented from 0.02 to 0.6% of all bacteria in the epilimnion and between 0.1 and 1% in the hypolimnion. These proportions were independently confirmed using catalyzed reporter deposition-fluorescence <i>in situ</i> hybridization (CARD-FISH). Some cells in the epilimnion were attached to diatoms (<i>Fragilaria</i> sp.) or cyanobacteria (<i>Microcystis</i> sp.), which suggests a close association with phytoplankton. In addition, we reconstructed 45 metagenome-assembled genomes (MAGs) related to <i>Gemmatimonadota</i> They represent several novel lineages, which persist in the studied lakes during the seasons. Three lineages contained photosynthesis gene clusters. One of these lineages was related to <i>Gemmatimonas phototrophica</i> and represented the majority of <i>Gemmatimonadota</i> retrieved from the lakes' epilimnion. The other two lineages came from hypolimnion and probably represented novel photoheterotrophic genera. None of these phototrophic MAGs contained genes for carbon fixation. Since most of the identified MAGs were present during the whole year and cells associated with phytoplankton were observed, we conclude that they represent truly limnic <i>Gemmatimonadota</i> distinct from the previously described species isolated from soils or sediments.<b>IMPORTANCE</b> Photoheterotrophic bacterial phyla such as <i>Gemmatimonadota</i> are key components of many natural environments. Its first photoheterotrophic cultured member, <i>Gemmatimonas phototrophica</i>, was isolated in 2014 from a shallow lake in the Gobi Desert. It contains a unique type of photosynthetic complex encoded by a set of genes which were likely received via horizontal transfer from <i>Proteobacteria</i> We were intrigued to discover how widespread this group is in the natural environment. In the presented study, we analyzed 45 metagenome-assembled genomes (MAGs) that were obtained from five freshwater lakes in Switzerland and Czechia. Interestingly, it was found that phototrophic <i>Gemmatimonadota</i> are relatively common in euphotic zones of the studied lakes, whereas heterotrophic <i>Gemmatimonadota</i> prevail in deeper waters. Moreover, our analysis of the MAGs documented that these freshwater species contain almost the same set of photosynthesis genes identified before in <i>Gemmatimonas phototrophica</i> originating from the Gobi Desert.