Award: OCE-1459600

Overview. Iron is a critical element for life that serves as an essential trace element for eukaryotic organisms, while it is common in sediments it is a key limiting nutrient in the upper water column in a third of the global ocean. Understanding biological controls on the iron cycle is thus important to understanding the mechanism behind this nutrient limitation, as well as understanding important sediment biogeochemistry. Conventional wisdom holds that most of the iron oxidation in sediments is abiological, as a result of the rapid kinetics of chemical iron oxidation in the presence of oxygen. The central premise of this work was that conventional wisdom is incorrect, iron oxidation is primarily biological, and that microbes play an essential role in iron oxidation, thereby influencing the marine iron-cycle and iron availability to the ocean. Iron-oxidizing microbes are able to support all their growth requirements by extracting energy from the oxidation of iron and fixing carbon dioxide. Our previous work has shown they are important at hydrothermal vents in the ocean, but little was known about their distribution or abundance in sediments. We carried out surveys of marine sediments for the presence of the Zetaproteobacteria a well-known group of iron-oxidizers, followed a seasonal cycle in an intertidal sediment, and conducted laboratory mesocosm experiments to understand the role of hypoxia or low oxygen conditions on iron-cycling in sediments. Intellectual Merit. An initial significant finding was that visible iron oxidation in marine sediments was almost exclusively associated with bioturbating macrofauna, principally polychaete worms in the sampling sties we examined. In bulk sediments with bioturbation, the abundance of Zetaproteobacteria ranged from below detection to around 1% of the population in bulk sediment, whereas in worm burrow walls in these sediments abundances ranged from 0.1% - 15% indicating the partitoning of iron-oxidizers to worm burrow walls. From our own work and analyzing global metagenome data for marine sediments, we estimated Zetaproteobacteria represent an average of 1.05 x 1026 cells (3.83 x1024-1.44 x 1027) in the upper 10 cm of continental shelf sediments, and annual sedimentary biological oxidation of iron—forming iron oxides—could exceed the annual flux of iron oxides from rivers to coastal sediments by up to a factor of ten, primarily due to iron recycling. Following on this work we conducted a seasonal study linking iron geochemistry and microbial population dynamics along with presence of marine worms. Both dissolved and solid phase iron pools correlated positively with temperature over the season—increases in the sediment temperature resulted in increases in both iron pools. We attribute these increases to the enhanced activity of bioturbating macrofauna in this mudflat, with increased respiration and burrow irrigation at elevated temperature. Building on the above field studies, we conducted controlled laboratory mesocosm experiments to test the effect of declining oxygen—hypoxia—on the iron biogeochemical cycle in bioturbated coastal sediments. In all cases there were dramatic differences in mesocosms with Nereus diversicolor a common marine worm, and those without. Mesocosms with worms present had a significantly greater flux of iron to the water column and different microbial communities, except under very hypoxic conditions where the worms did not survive. In addition to these environmental studies we have also sequenced the genomes of three new isolates of Fe-oxidizing Zetaproteobacteria from marine sediments. Each isolate belongs to a novel clade, including those that we see as most representative of those present in coastal sediments. One of these strains has a number of significant differences in it's electron transport chain for growing on iron, indicating it has a unique physiology, likely adapted for it's sedimentary habitat. Broader Impacts. Our results systematically show, for the first time, the presence of iron-oxidizing bacteria, principally the Zetaproteobacteria, in coastal marine sediments, and provide estimates for their global importance in an active iron cycle. They also demonstrate the direct association of iron-oxidizing communities with bioturbating macrofauna. Direct linkages between bioturbating animals and microbial populations that result in important functional activities is a poorly understood phenomena in benthic microbial ecology. This work has also quantitated the effects of hypoxia on iron release from the sediments using manipulative laboratory experiments. An important impact of climate change on marine environments is a predicted increase in low O2 or hypoxic zones in the ocean. These experiments will help in predictions of how those conditions may impact the marine iron cycle, which in turn impacts productivity in the ocean. The project resulted in training for a postdoctoral scientist, ongoing collaborations with faculty, and Ph.D students at Harvard University a collaborating institution on the project, and training for 4 undergraduate students. There have been 13 publications and presentations at national or international meeting supported by the project, several more publications are in preparation. Data from the project has been distributed to the sequence read archive at Genbank, the Integrated Microbial Genome database, and BCO-DMO (https://www.bco-dmo.org/project/544584). Last Modified: 06/01/2018 Submitted by: David Emerson