Common Presence of Phototrophic Gemmatimonadota in Temperate Freshwater Lakes

Abstract

Members of the bacterial phylum Gemmatimonadota are ubiquitous in most natural environments and represent one of the top 10 most abundant bacterial phyla in soil. Sequences affiliated with Gemmatimonadota 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, Gemmatimonadota 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 in situ hybridization (CARD-FISH). Some cells in the epilimnion were attached to diatoms (Fragilaria sp.) or cyanobacteria (Microcystis sp.), which suggests a close association with phytoplankton. In addition, we reconstructed 45 metagenome-assembled genomes (MAGs) related to Gemmatimonadota. 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 Gemmatimonas phototrophica and represented the majority of Gemmatimonadota 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 Gemmatimonadota distinct from the previously described species isolated from soils or sediments. IMPORTANCE Photoheterotrophic bacterial phyla such as Gemmatimonadota are key components of many natural environments. Its first photoheterotrophic cultured member, Gemmatimonas phototrophica, 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 Proteobacteria. 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 Gemmatimonadota are relatively common in euphotic zones of the studied lakes, whereas heterotrophic Gemmatimonadota 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 Gemmatimonas phototrophica originating from the Gobi Desert.

Phylum Gemmatimonadota and Its Role in the Environment

“…The figure was adapted from ref. [18]. (b) Absorption spectra of two cultures G. phototrophica (black) and G. groenlandica (red).…”

“…Interestingly, Gemmatimonadota dominated in alkaline [86] and highly saline soils and represented almost 17% of all bacterial reads [87]. Maximum-likelihood phylogeny of 16S rRNA genes of Gemmatimonadota sequences recovered from the SILVA SSU v138 database (in total, 169 sequences, >1200 bp, sequence quality >94%, downloaded on 23 November 2021), 36 16S rRNA gene sequences whose accession numbers were taken from [22,59], and 12 sequences taken from [18]. All of the accession numbers are provided as Supplement Table S1.…”

“…In contrast to the low number of described species, culture-independent methods indicate that members of Gemmatimonadota are ubiquitous and especially common in soils, limnic environments, and sediments [17]. Metagenomic analyses documented unexpected phylogenomic and metabolic diversity among uncultured Gemmatimonadota [18]. Moreover, several lineages of this phylum are capable of anoxygenic photosynthesis [15,16,19].…”

The Relationship between the Community Structure and Function of Bacterioplankton and the Environmental Response in Qingcaosha Reservoir

“…Sphingomonadales is responsible for ammonia oxidation and its abundance is positively correlated with the abundance of Melosira granulata, while the abundance of Gemmataceae in the reservoir is negatively correlated with it. Gemmataceae is closely related to Phytoplankton, and is mainly attached to Diatoms and Cyanobacteria [51]. Gemmataceae has a strong phosphorus accumulation ability [52] and is an important genus in the process of biological phosphorus removal from wastewater [53].…”

Structure elucidation of the novel carotenoid gemmatoxanthin from the photosynthetic complex of Gemmatimonas phototrophica AP64

“…The phylum Gemmatimonadetes was formally established in 2003, with Gemmatimonas (G.) aurantiaca as the type species. Even though there exists only a handful of cultured strains, Gemmatimonadetes are known to be relatively common organisms in many natural habitats, such as soils, sediments and freshwaters 3,4 . To date, two phototrophic species have been described in the genus Gemmatimonas: G. phototrophica AP64, originating from a freshwater lake in the Gobi Desert 5 , and G. groenlandica TET16 isolated from a freshwater stream in Greenland 6 .…”