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Aerobic and anaerobic iron oxidizers together drive denitrification and carbon cycling at marine iron-rich hydrothermal vents.

ABSTRACT: In principle, iron oxidation can fuel significant primary productivity and nutrient cycling in dark environments such as the deep sea. However, we have an extremely limited understanding of the ecology of iron-based ecosystems, and thus the linkages between iron oxidation, carbon cycling, and nitrate reduction. Here we investigate iron microbial mats from hydrothermal vents at Lō'ihi Seamount, Hawai'i, using genome-resolved metagenomics and metatranscriptomics to reconstruct potential microbial roles and interactions. Our results show that the aerobic iron-oxidizing Zetaproteobacteria are the primary producers, concentrated at the oxic mat surface. Their fixed carbon supports heterotrophs deeper in the mat, notably the second most abundant organism, Candidatus Ferristratum sp. (uncultivated gen. nov.) from the uncharacterized DTB120 phylum. Candidatus Ferristratum sp., described using nine high-quality metagenome-assembled genomes with similar distributions of genes, expressed nitrate reduction genes narGH and the iron oxidation gene cyc2 in situ and in response to Fe(II) in a shipboard incubation, suggesting it is an anaerobic nitrate-reducing iron oxidizer. Candidatus Ferristratum sp. lacks a full denitrification pathway, relying on Zetaproteobacteria to remove intermediates like nitrite. Thus, at Lō'ihi, anaerobic iron oxidizers coexist with and are dependent on aerobic iron oxidizers. In total, our work shows how key community members work together to connect iron oxidation with carbon and nitrogen cycling, thus driving the biogeochemistry of exported fluids.

SUBMITTER: McAllister SM

PROVIDER: S-EPMC8114936 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Zetaproteobacteria create extensive iron (Fe) oxide mats at marine hydrothermal vents, making them an ideal model for microbial Fe oxidation at circumneutral pH. Comparison of neutrophilic Fe oxidizer isolate genomes has revealed a hypothetical Fe oxidation pathway, featuring a homolog of the Fe oxidase Cyc2 from Acidithiobacillus ferrooxidans However, Cyc2 function is not well verified in neutrophilic Fe oxidizers, particularly in Fe-oxidizing environments. Toward this, we analyzed genomes and metatranscriptomes of Zetaproteobacteria, using 53 new high-quality metagenome-assembled genomes reconstructed from Fe mats at Mid-Atlantic Ridge, Mariana Backarc, and Loihi Seamount (Hawaii) hydrothermal vents. Phylogenetic analysis demonstrated conservation of Cyc2 sequences among most neutrophilic Fe oxidizers, suggesting a common function. We confirmed the widespread distribution of cyc2 and other model Fe oxidation pathway genes across all represented Zetaproteobacteria lineages. High expression of these genes was observed in diverse Zetaproteobacteria under multiple environmental conditions and in incubations. The putative Fe oxidase gene cyc2 was highly expressed in situ, often as the top expressed gene. The cyc2 gene showed increased expression in Fe(II)-amended incubations, with corresponding increases in carbon fixation and central metabolism gene expression. These results substantiate the Cyc2-based Fe oxidation pathway in neutrophiles and demonstrate its significance in marine Fe-mineralizing environments.IMPORTANCE Iron oxides are important components of our soil, water supplies, and ecosystems, as they sequester nutrients, carbon, and metals. Microorganisms can form iron oxides, but it is unclear whether this is a significant mechanism in the environment. Unlike other major microbial energy metabolisms, there is no marker gene for iron oxidation, hindering our ability to track these microbes. Here, we investigate a promising possible iron oxidation gene, cyc2, in iron-rich hydrothermal vents, where iron-oxidizing microbes dominate. We pieced together diverse Zetaproteobacteria genomes, compared these genomes, and analyzed expression of cyc2 and other hypothetical iron oxidation genes. We show that cyc2 is widespread among iron oxidizers and is highly expressed and potentially regulated, making it a good marker for the capacity for iron oxidation and potentially a marker for activity. These findings will help us understand and potentially quantify the impacts of neutrophilic iron oxidizers in a wide variety of marine and terrestrial environments.

Project description:To elucidate the potential for nitrification and denitrification processes in a high latitude deep oxygen minimum zone (OMZ) we determined the abundance and community composition of the main microbial players in the aerobic and anaerobic (anammox) ammonium oxidation and denitrification processes in the Gulf of Alaska throughout the water column. Within the dominant bacterial groups, Flavobacterales, Rhodobacterales, Actinomarinales, and SAR86 were more abundant in epipelagic waters and decreased with depth, whereas SAR11, SAR324, Marinimicrobia, and Thiomicrospirales increased their contribution to the bacterial community with depth. Nitrosopumilaceae also increased with depth and dominated the OMZ and bathypelagic archaeal communities. Euryarchaeota Marine Group II exhibited an opposite depth pattern to Nitrosopumilaceae, whereas Marine Group III and Woesearchaeota were more abundant in the bathypelagic realm. Candidatus Brocadia contributed 70-100% of the anammox bacterial community throughout the water column. Archaeal ammonia oxidizers (AOA) dominated the microbial community involved in the nitrogen cycle. Two AOA ecotypes, the high ammonia (HAC) and low ammonia (LAC)-AOA, characterized by distinct genes for aerobic ammonia oxidation (amoA) and for denitrification (nirK), exhibited a distinct distribution pattern related to depth and ammonia concentrations. HAC-AOA dominated in epipelagic (80.5 ± 28.3% of total AOA) oxygenated and ammonia-rich waters, and LAC-AOA dominated in the OMZ (90.9 ± 5.1%) and bathypelagic waters (85.5 ± 13.5%), characterized by lower oxygen and ammonia concentrations. Bacterial denitrifiers (3.7 ± 6.9 bacterial nirK gene mL-1) and anaerobic ammonia oxidizers (78 ± 322 anammox 16S rRNA genes L-1) were low in abundance under the oxygen conditions in the Gulf of Alaska throughout the water column. The widespread distribution of bacterial denitrifiers and anaerobic ammonia oxidizers in low abundances reveals a reservoir of genetic and metabolic potential ready to colonize the environment under the predicted increase of OMZs in the ocean. Taken together, our results reinforce the niche partitioning of archaeal ammonia oxidizers based on their distinct metabolic characteristics resulting in the dominance of LAC-AOA in a high latitude deep OMZ. Considering the different ecological roles and functions of the two archaeal ecotypes, the expansion of the zones dominated by the LAC-ecotype might have implications for the nitrogen cycle in the future ocean.

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Aerobic and anaerobic iron oxidizers together drive denitrification and carbon cycling at marine iron-rich hydrothermal vents.

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