Diel cycle of lanthanide-dependent methylotrophy by TMED127/Methylaequorales bacteria in oligotrophic surface seawater

Abstract

Methanol, the simplest alcohol, has long been recognized as a key energy and carbon source for soil and plant-associated bacteria and fungi, and is increasingly recognized as an important substrate for marine bacteria. Lanthanide-dependent methanol dehydrogenases (encoded by the gene xoxF) are now recognized as the key catalysts for methylotrophy in many environments, yet the identity of the most transcriptionally active methylotrophs in open ocean waters ("Clade X") has remained elusive. Here we show that "Clade X" methylotrophs belong to the deep-branching alphaproteobacterial order TMED127, which we propose be renamed Methylaequorales; methyl for methylotrophic metabolism and aequor for ocean surface, as these bacteria are most transcriptionally active near the sea surface. TMED127/Methylaequorales are present in surface waters of tropical and subtropical oceans throughout the global ocean. They have small, streamlined genomes ([~]1.5 Mb), and appear to be obligate methylotrophs that use the serine cycle for carbon assimilation. They display a diel pattern of xoxF5 and glucose dehydrogenase (gdh) transcription, peaking in the late afternoon, in oligotrophic surface water of the Sargasso Sea. Several other highly transcribed genes of unknown function had no homologs outside of TMED127/Methylaequorales genomes. Our findings illuminate an overlooked marine methylotrophic bacterium and predict a diel cycle of methanol production in surface seawater by an unknown pathway. ImportanceMethanol metabolism is increasingly recognized as an important process in the marine carbon cycle, yet the identity and metabolism of the microorganisms mediating methylotrophy in the open ocean have remained unknown. This study reveals that bacteria in the TMED127 order of Alphaproteobacteria, proposed new name of "Methylaequorales", abundantly transcribe the key gene for lanthanide-dependent methylotrophy in oligotrophic surface waters of the worlds oceans. TMED127/Methylaequorales likely require methanol as a carbon and energy source and display a diel pattern of transcription of key genes for methylotrophy that peaks in the late afternoon. These findings motivate future studies on the mechanisms of methanol production in surface seawater.