Active, novel and unexpected methanotrophs play a key role in methane oxidation in the Gulf of Mexico hypoxic zone

Katie Howe, Florida State University, Tallahassee, United States, Kiley Seitz, University of Texas at Austin, Austin, TX, United States, Lauren Gillies, Florida State University, Earth, Ocean and Atmosphere Department, Tallahassee, FL, United States, Brett J Baker, University of Texas at Austin, United States, Cameron Cameron Thrash, University of Southern California, Department of Biological Sciences, Los Angeles, United States, Nancy N Rabalais, Louisiana State University, Oceanography and Coastal Sciences, Baton Rouge, LA, United States, Mary Katherine Rogener, University of Georgia, Marine Sciences, Athens, GA, United States, Samantha Benton Joye, Univ Georgia, Department of Marine Sciences, Athens, GA, United States and Olivia Mason, Florida State University, Earth, Ocean, and Atmospheric Department, Tallahassee, United States
Abstract:
The annual oxygen minimum zone in the northern Gulf of Mexico (nGOM) is the second largest human-caused dead zone in the world. In this dead zone oxygen depleted, methane-rich water is trapped at depth due to thermal stratification. To determine the microorganisms that actively mediate methane oxidation in bottom water, methane oxidation rates were determined and 16S rRNA gene (iTag), metagenome and metatranscriptome sequencing and bioinformatics analyses were carried out. Few canonical methanotrophs were detected in the iTag data, yet methane monooxygenase (pmoA) was one of the most highly expressed transcripts in the unassembled metatranscriptome data. Metagenome-assembled genomes (MAGs) from the 2013 nGOM dead zone were obtained and annotated with six MAGs encoding at least one pmoA gene copy. These MAGs were classified as Planctomycetaceae, Verrucomicrobiales, and one unclassified Bacteria, putatively identified as Latescibacteria and represent novel, non-canonical marine methanotrophs. Further analysis of these six MAGs, TARA Oceans MAGs, and other MAGs and isolates with available genomes provide additional support that members of the phyla Verrucomicrobia and Planctomycetes, as well as Candidate phylum Poribacteria, are active, aerobic marine methanotrophs. This indicates that there is a large, diverse, and unrecognized community of active aerobic methanotrophs in the nGOM dead zone acting as a biofilter by mitigating methane flux to the atmosphere. This also suggests that previously unrecognized methanotrophs may be critical in regulating methane flux in other marine environments.