Discovery of Seven New Encapsulin Nanocompartments Including Two from Anammox Bacteria

Bioinformatic techniques identified seven new protein nanocompartments, including two in nitrogen (N) transforming anammox bacteria. The biochemical role of these so called encapsulin nanocompartments in anammox N loss is unknown; however, the putative identities of enzymes associated with these compartments suggest that they may be involved in the three step anammox process. N is essential for life, yet most life cannot utilize the abundant dinitrogen gas in Earth's atmosphere. As a result, the microbial pathways that control the availability of fixed N often constrain primary productivity in terrestrial and marine environments. Many microbes deploy protein compartments, such as ferritins, bacterial microcompartments, or encapsulins, to store nutrients, counteract redox stress, mediate toxicity, and optimize metabolic reactions. Freshwater anammox encapsulin systems contain cargo enzymes putatively involved in the nitrogen transformations of the anammox process. Published Scalindua draft genomes and environmental metagenomes from marine oxygen minimum zones (OMZs) were searched for marine anammox encapsulins. Through these searches a novel Scalindua encapsulin system with a putative nitrite reductase cargo enzyme was identified in Scalindua rubra, an unusual species adapted to a brine pool ecosystem in the Red Sea. HMMER searches of additional environmental metagenomes returned six novel encapsulins across diverse bacterial phyla. These six encapsulins include an additional freshwater anammox encapsulin identified in Brocadia caroliniensis. These results provide further evidence that encapsulin nanocompartments are a widespread microbial adaptation that grant prokaryotes some of the advantages of eukaryotic cellular compartmentalization. These results also lay the groundwork for current studies we are performing to explore the biochemistry of anammox encapsulins to determine if they play a role in N loss.