EAGER: Did Oxygenic Photosynthesis Cause Marine Group 1 Crenarchaeota to Take a Dive?

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The presence of hydrogen peroxide in surface seawater is tied to solar radiation and its concentration varies seasonally as well as diurnally. H2O2 concentrations in the environment are low relative to those tolerated by many Bacteria, but relative to Bacteria, marine group 1 Crenarchaeota (MG1C) appear to lack defenses against it. Thus, photic zone concentrations of H2O2 may be sufficient to inhibit MG1C metabolism if they have not developed alternative strategies for mitigating H2O2 toxicity, for example by eliminating, replacing or protecting sensitive targets in the cell with structures that are less susceptible to H2O2 poisoning. Given that only 2 MG1C genomes have been sequenced and that these sequences have not been fully annotated, let alone had the annotations verified experimentally, it is difficult to infer from genomic evidence whether MG1C have other adaptations for dealing with H2O2 in the environment. Thus, this project will to address this question directly by testing MG1C sensitivity to H2O2 by combining toxicity bioassays of mesopelagic plankton assemblages with MicroAutoRadiography-Fluorescent In Situ Hybridization (MAR-FISH) to identify target groups. If the proposed experiments verify that MG1C are sensitive to H2O2, this property of MG1C could answer a number of questions. 1) The global and seasonal distributions of MG1C - why they do not live in the surface layer; their seasonal distribution at high latitudes; and their distributions relative to Euryarchaeota, which have more catalases and peroxidases and are more common in surface waters and nearshore environments. 2) Substrate utilization and metabolism patterns - if they are sensitive to it, MG1C can only use substrates or metabolize via pathways that do not generate H2O2. 3) Lack of Archaeal pathogens - a burst of reactive oxygen species (ROS) is an animal host's first line of defense against pathogens. 4) Why MG1C are hard to culture - many standard lab practices generate ROS; this may apply to Bacteria that have proven hard to culture as well, as not all Bacteria have catalase or peroxidase genes. 5) The divergence between Bacteria and Archaea - peroxide sensitivity may result from a "frozen metabolic accident" that was a fundamental property of Archaeal biochemistry at about the time that oxygenic photosynthesis evolved. 6) Some of the biochemical and compositional differences between Bacteria and Archaea - one way some Bacteria have adapted to high-ROS lifestyles has been to eliminate or protect ROS targets in their cellular machinery.This is a pilot project of limited scope and budget. Nonetheless it will contribute directly to graduate and undergraduate education. Results will be disseminated via publications and presentations at meetings and in the classroom, and data will be made publicly available in accordance with NSF's data release policy. Although the problem is important and that the arguments and evidence in favor of the hypothesis are provocative and convincing, they are circumstantial, speculative and would not pass the test of peer-review. The implications of the hypothesis are transformative, however, and this project would allow a limited test of this hypothesis.