Microbiome of the deep Lake Baikal, a unique oxic bathypelagic habitat

Abstract

Lake Baikal is the deepest lake in the world. Its depth provides the only bathypelagic (> 1000 m deep) freshwaterhabitat on Earth and its oxic, ultra-oligotrophic features make it a freshwater counterpart of the deep ocean. Herewe have analyzed metagenomes from 1250 and 1350 m deep samples and built 231 metagenome-assembledgenomes (MAGs). We detected high fractions of Thaumarchaeota (ca. 20% of 16S rRNA reads) and members of thecandidate phyla radiation (CPR) (3–4.5%). Among the MAGs, we obtained ammonia-oxidizing archaea (AOA,Nitrosopumilaceae) and bacteria (AOB, Nitrosomonadaceae), and nitrite-oxidizers (Nitrospirae) indicating veryactive nitrification. A new clade of freshwater SAR202 Chloroflexi and methanotrophs (Methyloglobulus) were alsoremarkably abundant, the latter reflecting a possible role of methane oxidation as well. Novel species of streamlinedand cosmopolitan bacteria such as Ca. Fonsibacter or acI Actinobacteria were more abundant at the surface but alsopresent in deep waters. Conversely, CPRs, Myxococcales, Chloroflexi, DPANN (Diapherotrites, Parvarchaeota,Aenigmarchaeota, Nanoarchaeota and Nanohaloarchaeota) archaea, or Gammaproteobacteria were found only inbathypelagic samples. We noted various important taxonomic and metabolic differences between deep aphoticregion of Lake Baikal and marine waters of similar depth: Betaproteobacteriales, CPR, and DPANN superphylumwere only found in bathypelagic Baikal, while Deltaproteobacteria, Gammaproteobacteria, or Alphaproteobacteriaprevailed in oceanic samples. The genes mediating ammonia and methane oxidation, aromatic compound degra-dation, or alkane/methanesulfonate monooxygenases were detected in higher numbers in deep Baikal compared totheir oceanic counterparts or its own surface. Overall, depth seems to be less relevant than salinity in configuringthe microbial community.