Marine Fe-oxidizing<i>Zetaproteobacteria</i>: Historical, ecological, and genomic perspectives

McAllister, Sean M.; Rm, Moore; Gartman, Amy; Luther, George W.; Emerson, David; Chan, Clara S.

doi:10.1101/416842

Cited by 8 publications

(12 citation statements)

References 110 publications

(173 reference statements)

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“…Fe-oxyhydroxide deposits in modern low-temperature hydrothermal environments on the seafloor commonly host Fe-oxidizing Zetaproteobacteria (e.g., Emerson & Moyer, 2002;Forget, Murdock, & Juniper, 2010;Kato, Kobayashi, Kakegawa, & Yamagishi, 2009;Li et al, 2012;McAllister et al, 2019;Scott, Breier, Luther, & Emerson, 2015), which actively contribute to the growth of the deposits through biomineralization and stalk formation (e.g., Alt, 1988;Boyd & Scott, 2001;Edwards et al, 2011;Juniper & Fouquet, 1988;Karl, Brittain, & Tilbrook, 1989;Kennedy, Scott, & Ferris, 2003;Langley et al, 2009). These deposits may be similar to the sedimentary precursors of jaspers and iron formations, both with respect to mineralogy and genesis.…”

Section: Introductionmentioning

confidence: 99%

On the biogenicity of Fe‐oxyhydroxide filaments in silicified low‐temperature hydrothermal deposits: Implications for the identification of Fe‐oxidizing bacteria in the rock record

et al. 2019

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Microaerophilic Fe(II)‐oxidizing bacteria produce biomineralized twisted and branched stalks, which are promising biosignatures of microbial Fe oxidation in ancient jaspers and iron formations. Extracellular Fe stalks retain their morphological characteristics under experimentally elevated temperatures, but the extent to which natural post‐depositional processes affect fossil integrity remains to be resolved. We examined siliceous Fe deposits from laminated mounds and chimney structures from an extinct part of the Jan Mayen Vent Fields on the Arctic Mid‐Ocean Ridge. Our aims were to determine how early seafloor diagenesis affects morphological and chemical signatures of Fe‐oxyhydroxide biomineralization and how extracellular stalks differ from abiogenic features. Optical and scanning electron microscopy in combination with focused ion beam‐transmission electron microscopy (FIB‐TEM) was used to study the filamentous textures and cross sections of individual stalks. Our results revealed directional, dendritic, and radial arrangements of biogenic twisted stalks and randomly organized networks of hollow tubes. Stalks were encrusted by concentric Fe‐oxyhydroxide laminae and silica casings. Element maps produced by energy dispersive X‐ray spectroscopy (EDS) in TEM showed variations in the content of Si, P, and S within filaments, demonstrating that successive hydrothermal fluid pulses mediate early diagenetic alteration and modify the chemical composition and surface features of stalks through Fe‐oxyhydroxide mineralization. The carbon content of the stalks was generally indistinguishable from background levels, suggesting that organic compounds were either scarce initially or lost due to percolating hydrothermal fluids. Dendrites and thicker abiotic filaments from a nearby chimney were composed of nanometer‐sized microcrystalline iron particles and silica and showed Fe growth bands indicative of inorganic precipitation. Our study suggests that the identification of fossil stalks and sheaths of Fe‐oxidizing bacteria in hydrothermal paleoenvironments may not rely on the detection of organic carbon and demonstrates that abiogenic filaments differ from stalks and sheaths of Fe‐oxidizing bacteria with respect to width distribution, ultrastructure, and textural context.

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Section: Introductionmentioning

confidence: 99%

On the biogenicity of Fe‐oxyhydroxide filaments in silicified low‐temperature hydrothermal deposits: Implications for the identification of Fe‐oxidizing bacteria in the rock record

et al. 2019

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“…Mariana mats had shallow O 2 gradients while at Loihi, O 2 was undetectable (<3 µM) at 1 cm below the mat surface. These Fe(II) and O 2 conditions favor biotic Fe oxidation [10]. At Mariana, total dissolved Fe was depleted by 49%-74% in our low temperature mats relative to the conservative mixing of the local high-temperature zero-Mg endmember ( Supplemental Figure 2 ), which suggests that a substantial amount of Fe is being oxidized and precipitated within these mats.…”

Section: Resultsmentioning

confidence: 82%

“…Comparative genomics has led to multiple proposed pathways, each involving an outer membrane cytochrome [5–7]. However, only one pathway is present in all well-established neutrophilic Fe-oxidizing isolates (Zetaproteobacteria and Gallionellaceae), centering on a fused cytochrome-porin Cyc2 [7–10]. Yet, beyond comparative genomics, we lack evidence of the Cyc2 pathway function in neutrophilic Fe-oxidizers, particularly the uncultured Fe-oxidizers that dominate natural Fe systems.…”

Section: Introductionmentioning

confidence: 99%

“…To this end, we turned to Zetaproteobacteria in natural Fe microbial mats. The Zetaproteobacteria discovered to date are all considered to be Fe-oxidizers, since every isolate grows by Fe oxidation and uncultured Zetaproteobacteria are typically found in Fe-oxidizing environments [10, 16–21]. The Zetaproteobacteria are often the dominant organisms in marine hydrothermal Fe mats [22–25], where they play a key role in mat formation [26].…”

Section: Introductionmentioning

confidence: 99%

“…We sampled paired metagenomes and metatranscriptomes from three hydrothermal venting regions: Loihi Seamount, the Mid-Atlantic Ridge (Rainbow, TAG, and Snake Pit vents), and the Mariana Backarc (Urashima vent field). Recovery of high quality metagenome assembled genomes (MAGs) allowed us to improve the limited genomic representation of the Zetaproteobacteria (see [10] for a summary). Using the MAGs for reference mapping, we explored in situ environmental expression of the Zetaproteobacteria within undisturbed natural Fe mats.…”

Section: Introductionmentioning

confidence: 99%

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Validating the Cyc2 neutrophilic Fe oxidation pathway using meta-omics of Zetaproteobacteria iron mats at marine hydrothermal vents

McAllister

Polson

Butterfield

et al. 2019

Preprint

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27 Zetaproteobacteria create extensive iron (Fe) oxide mats at marine hydrothermal vents, making 28 them an ideal model for microbial Fe oxidation at circumneutral pH. Comparison of neutrophilic 29 Fe-oxidizer isolate genomes has revealed a hypothetical Fe oxidation pathway, featuring a 30 homolog of the Fe oxidase Cyc2 from Acidithiobacillus ferrooxidans. However, Cyc2 function is 31 not well verified in neutrophilic Fe-oxidizers, particularly in Fe-oxidizing environments. Toward 32 this, we analyzed genomes and metatranscriptomes of Zetaproteobacteria, using 53 new high-33 quality metagenome assembled genomes reconstructed from Fe mats at Mid-Atlantic Ridge, 34 Mariana Backarc, and Loihi Seamount (Hawaii) hydrothermal vents. Phylogenetic analysis 35 demonstrated conservation of Cyc2 sequences among most neutrophilic Fe-oxidizers, suggesting 36 a common function. We confirmed the widespread distribution of cyc2 and other model Fe 37 oxidation pathway genes across all represented Zetaproteobacteria lineages. High expression of 38

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Carbon fixation and energy metabolisms of a subseafloor olivine biofilm

et al. 2019

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Earth's largest aquifer ecosystem resides in igneous oceanic crust, where chemosynthesis and water-rock reactions provide the carbon and energy that support an active deep biosphere. The Calvin Cycle is the predominant carbon fixation pathway in cool, oxic, crust; however, the energy and carbon metabolisms in the deep thermal basaltic aquifer are poorly understood. Anaerobic carbon fixation pathways such as the Wood-Ljungdahl pathway, which uses hydrogen (H 2) and CO 2 , may be common in thermal aquifers since water-rock reactions can produce H 2 in hydrothermal environments and bicarbonate is abundant in seawater. To test this, we reconstructed the metabolisms of eleven bacterial and archaeal metagenome-assembled genomes from an olivine biofilm obtained from a Juan de Fuca Ridge basaltic aquifer. We found that the dominant carbon fixation pathway was the Wood-Ljungdahl pathway, which was present in seven of the eight bacterial genomes. Anaerobic respiration appears to be driven by sulfate reduction, and one bacterial genome contained a complete nitrogen fixation pathway. This study reveals the potential pathways for carbon and energy flux in the deep anoxic thermal aquifer ecosystem, and suggests that ancient H 2-based chemolithoautotrophy, which once dominated Earth's early biosphere, may thus remain one of the dominant metabolisms in the suboceanic aquifer today.

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Marine Fe-oxidizingZetaproteobacteria: Historical, ecological, and genomic perspectives

Abstract: 18

Cited by 8 publications

References 110 publications

On the biogenicity of Fe‐oxyhydroxide filaments in silicified low‐temperature hydrothermal deposits: Implications for the identification of Fe‐oxidizing bacteria in the rock record

On the biogenicity of Fe‐oxyhydroxide filaments in silicified low‐temperature hydrothermal deposits: Implications for the identification of Fe‐oxidizing bacteria in the rock record

Validating the Cyc2 neutrophilic Fe oxidation pathway using meta-omics of Zetaproteobacteria iron mats at marine hydrothermal vents

Carbon fixation and energy metabolisms of a subseafloor olivine biofilm

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