Freshwater Chlorobia Exhibit Metabolic Specialization among Cosmopolitan and Endemic Populations

• Published in: mSystems
• Main Authors: Garcia, Sarahi L., Mehrshad, Maliheh, Buck, Moritz, Tsuji, Jackson M., Neufeld, Josh D., McMahon, Katherine D., Bertilsson, Stefan, Greening, Chris, Peura, Sari
• Format: Text
• Language: English
• Published: American Society for Microbiology 2021
• Subjects: Research Article; Subarctic
• Online Access: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8125076/; http://www.ncbi.nlm.nih.gov/pubmed/33975970; https://doi.org/10.1128/mSystems.01196-20

Photosynthetic bacteria from the class Chlorobia (formerly phylum Chlorobi) sustain carbon fixation in anoxic water columns. They harvest light at extremely low intensities and use various inorganic electron donors to fix carbon dioxide into biomass. Until now, most information on the functional ecology and local adaptations of Chlorobia members came from isolates and merely 26 sequenced genomes that may not adequately represent natural populations. To address these limitations, we analyzed global metagenomes to profile planktonic Chlorobia cells from the oxyclines of 42 freshwater bodies, spanning subarctic to tropical regions and encompassing all four seasons. We assembled and compiled over 500 genomes, including metagenome-assembled genomes (MAGs), single-amplified genomes (SAGs), and reference genomes from cultures, clustering them into 71 metagenomic operational taxonomic units (mOTUs or “species”). Of the 71 mOTUs, 57 were classified within the genus Chlorobium, and these mOTUs represented up to ∼60% of the microbial communities in the sampled anoxic waters. Several Chlorobium-associated mOTUs were globally distributed, whereas others were endemic to individual lakes. Although most clades encoded the ability to oxidize hydrogen, many lacked genes for the oxidation of specific sulfur and iron substrates. Surprisingly, one globally distributed Scandinavian clade encoded the ability to oxidize hydrogen, sulfur, and iron, suggesting that metabolic versatility facilitated such widespread colonization. Overall, these findings provide new insight into the biogeography of the Chlorobia and the metabolic traits that facilitate niche specialization within lake ecosystems. IMPORTANCE The reconstruction of genomes from metagenomes has helped explore the ecology and evolution of environmental microbiota. We applied this approach to 274 metagenomes collected from diverse freshwater habitats that spanned oxic and anoxic zones, sampling seasons, and latitudes. We demonstrate widespread and abundant distributions of ...