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  1. Abstract

    The discharge of hydrothermal vents on the seafloor provides energy sources for dynamic and productive ecosystems, which are supported by chemosynthetic microbial populations. These populations use the energy gained by oxidizing the reduced chemicals contained within the vent fluids to fix carbon and support multiple trophic levels. Hydrothermal discharge is ephemeral and chemical composition of such fluids varies over space and time, which can result in geographically distinct microbial communities. To investigate the foundational members of the community, microbial growth chambers were placed within the hydrothermal discharge at Axial Seamount (Juan de Fuca Ridge), Magic Mountain Seamount (Explorer Ridge), and Kamaʻehuakanaloa Seamount (Hawai'i hotspot). Campylobacteria were identified within the nascent communities, but different amplicon sequence variants were present at Axial and Kamaʻehuakanaloa Seamounts, indicating that geography in addition to the composition of the vent effluent influences microbial community development. Across these vent locations, dissolved iron concentration was the strongest driver of community structure. These results provide insights into nascent microbial community structure and shed light on the development of diverse lithotrophic communities at hydrothermal vents.

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  2. Abstract

    In the past decade, thousands of previously unknown methane seeps have been identified on continental margins around the world. As we have come to appreciate methane seep habitats to be abundant components of marine ecosystems, we have also realized they are highly dynamic in nature. With a focus on discrete depth ranges across the Cascadia Margin, we work to further unravel the drivers of seep‐associated microbial community structure. We found highly heterogenous environments, with depth as a deterministic factor in community structure. This was associated with multiple variables that covaried with depth, including surface production, prevailing oxygen minimum zones (OMZs), and geologic and hydrographic context. Development of megafaunal seep communities appeared limited in shallow depth zones (~ 200 m). However, this effect did not extend to the structure or function of microbial communities. Siboglinid tubeworms were restricted to water depths > 1000 m, and we posit this deep distribution is driven by the prevailing OMZ limiting dispersal. Microbial community composition and distribution covaried most significantly with depth, but variables including oxygen concentration, habitat type, and organic matter, as well as iron and methane concentration, also explained the distribution of the microbial seep taxa. While members of the core seep microbiome were seen across sites, there was a high abundance of microbial taxa not previously considered within the seep microbiome as well. Our work highlights the multifaceted aspects that drive community composition beyond localized methane flux and depth, where environmental diversity adds to margin biodiversity in seep systems.

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  3. Abstract

    Current methods for biochemical and biogeochemical analysis of the deep-sea hydrothermal vent ecosystems rely on water sample recovery, orin situanalysis using underwater instruments with limited range of analyte detection and limited sensitivity. Even in cases where large quantities of sample are recovered, labile dissolved organic compounds may not be detected due to time delays between sampling and preservation. Here, we present a novel approach forin situextraction of organic compounds from hydrothermal vent fluids through a unique solid phase microextraction (SPME) sampler. These samplers were deployed to sample effluent of vents on sulphide chimneys, located on Axial Seamount in the North-East Pacific, in the Urashima field on the southern Mariana back-arc, and at the Hafa Adai site in the central Mariana back-arc. Among the compounds that were extracted, a wide range of unique organic compounds, including labile dissolved organic sulfur compounds, were detected through high-resolution LC-MS/MS, among which were biomarkers of anammox bacteria, fungi, and lower animals. This report is the first to show that SPME can contribute to a broader understanding of deep sea ecology and biogeochemical cycles in hydrothermal vent ecosystems.

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  4. ABSTRACT 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. 
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  5. Abstract

    Single‐celled microbial eukaryotes inhabit deep‐sea hydrothermal vent environments and play critical ecological roles in the vent‐associated microbial food web. 18S rRNA amplicon sequencing of diffuse venting fluids from four geographically‐ and geochemically‐distinct hydrothermal vent fields was applied to investigate community diversity patterns among protistan assemblages. The four vent fields include Axial Seamount at the Juan de Fuca Ridge, Sea Cliff and Apollo at the Gorda Ridge, all in the NE Pacific Ocean, and Piccard and Von Damm at the Mid‐Cayman Rise in the Caribbean Sea. We describe species diversity patterns with respect to hydrothermal vent field and sample type, identify putative vent endemic microbial eukaryotes, and test how vent fluid geochemistry may influence microbial community diversity. At a semi‐global scale, microbial eukaryotic communities at deep‐sea vents were composed of similar proportions of dinoflagellates, ciliates, Rhizaria, and stramenopiles. Individual vent fields supported distinct and highly diverse assemblages of protists that included potentially endemic or novel vent‐associated strains. These findings represent a census of deep‐sea hydrothermal vent protistan communities. Protistan diversity, which is shaped by the hydrothermal vent environment at a local scale, ultimately influences the vent‐associated microbial food web and the broader deep‐sea carbon cycle.

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  6. Abstract

    Mid‐ocean ridge eruptions, initiating or revitalizing hydrothermal discharge and disrupting seafloor ecosystems, occur regularly as a consequence of plate spreading. Evaluating their impact on long‐term hydrothermal discharge requires information on the scale and duration of any posteruption enhancement. Here we describe a unique hydrothermal plume time series of annual (or more frequent) observations at Axial Seamount vent fields from 1985 through 2017, missing only 7 years. Axial, a hot spot volcano astride the Juan de Fuca Ridge, experienced eruptions in 1998, 2011, and 2015. In 1998 and 2011 lava flooded the SE caldera and south rift zone, but in 2015 most lava was extruded in a series of flows extending ~20 km down the north rift zone. Response cruises occurred within 18 days (1998) to about 4 months, followed by regular posteruption observations. All 30 cruises measured plume rise height (a proxy for heat flux) and turbidity (indicative of chemical changes in vent discharge) at several vent sites, yielding an integrated view of vent field activity. Venting in the SE caldera area persisted throughout the time series, consistent with the imaged location of the shallowest portion of the melt‐rich magma reservoir. Eruptions produced substantial and diagnostic increases in plume rise and turbidity, and posteruption enhancements lasted 2–5 years, totaling ~10 years over the course of the time series. Estimates of the relative heat flux indicate a sixfold increase during eruption‐enhanced periods, implying that generalizations about mid‐ocean ridge hydrothermal fluxes may be underestimates if based on non–eruption‐enhanced hydrothermal activity alone.

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