Publications

2016
Schrader PS, Reimers CE, Girguis P, Delaney J, Doolan C, Wolf M, Green D. Independent benthic microbial fuel cells powering sensors and acoustic communications with the MARS underwater observatory. Journal of Atmospheric and Oceanic Technology. 2016;33 (3) :607–617.
Tang T, Mohr W, Sattin S, Rogers D, Girguis PR, Pearson A. Intracellular carbon isotope distributions of continuous-culture Allochromatium vinosum grown on acetate vs. CO 2. American Geophysical Union. 2016;2016 :MM44C–0508.
Sobol MS, Zinke LA, Orcutt B, Mills HJ, Edwards KJ, Girguis PR, Reese BK. Investigating the Differences in the Total and Active Microbial Community of Mid-Atlantic Ridge Sediments. American Geophysical Union. 2016;2016 :MM24B–0443.
Tully BJ, Heidelberg JF, Kraft B, Girguis PR, Huber JA. Metagenomic Assessment of a Dynamic Microbial Population from Subseafloor Aquifer Fluids in the Cold, Oxygenated Crust, in AGU Fall Meeting Abstracts. Vol 2016. ; 2016 :B13J–02.
Seston SL, Beinart RA, Sarode N, Shockey AC, Ranjan P, Ganesh S, Girguis PR, Stewart FJ. Metatranscriptional response of chemoautotrophic Ifremeria nautilei endosymbionts to differing sulfur regimes. Frontiers in microbiology. 2016;7 :1074.
Girguis P. Microbial ecology: Here, there and everywhere. Nature Microbiology. 2016;1 (8) :1–2.
Ge Z, Girguis PR, Buie CR. Nanoporous microscale microbial incubators. Lab on a Chip. 2016;16 (3) :480–488.
Padilla CC, Bristow LA, Sarode N, Garcia-Robledo E, Gómez Ram{\'ırez E, Benson CR, Bourbonnais A, Altabet MA, Girguis PR, Thamdrup B, et al. NC10 bacteria in marine oxygen minimum zones. The ISME journal. 2016;10 (8) :2067–2071.
Bradley AS, Leavitt WD, Schmidt M, Knoll AH, Girguis PR, Johnston DT. Patterns of sulfur isotope fractionation during microbial sulfate reduction. Geobiology. 2016;14 (1) :91–101.
Cordes E, Michel A, Petersen J, Wankel S, Ansorge R, Girguis P, Leisch N, Smart C, Roman C, Wetzel S, et al. ROV Hercules Investigates Brine Lakes on the Bottom of the Ocean. Oceanography. 2016;29 (1 Suppl. S) :30–31.
Fisher CR, Du Preez C, Ferrini VL, Beinart R, Seewald J, Hoer D, Girguis PR. Stability of Hydrothermal Vent Communities on the Eastern Lau Spreading Center, in AGU Fall Meeting Abstracts. Vol 2016. ; 2016 :OS34A–03.
Levin LA, Girguis PR, Brennan M, German CR, Raineault N, Le JT, Grupe B, Gallo N, Inderbitzen KE, Tuzun S, et al. (Tele) presenting Secrets from the Deep Southern California Margin. American Geophysical Union. 2016;2016 :ED24A–1655.
Picard A, Gartman A, Girguis PR. What do we really know about the role of microorganisms in iron sulfide mineral formation?. Frontiers in Earth Science. 2016;4 :68.
Maher WA, Duncan E, Dilly G, Foster S, Krikowa F, Lombi E, Scheckel K, Girguis P. Arsenic concentrations and species in three hydrothermal vent worms, Ridgeia piscesae, Paralvinella sulficola and Paralvinella palmiformis. Deep Sea Research Part I: Oceanographic Research Papers. 2016;116 :41 - 48. Publisher's VersionAbstract
Abstract Hydrothermal vents are surficial expressions of subsurface geological and hydrological processes. Fluids emitting from active vents are chemically distinct from bottom seawater, and are enriched in dissolved metals and metalloids, including arsenic. Vent organisms accumulate arsenic but the arsenic speciation in these non-photosynthetic organisms is largely unknown. Here, arsenic concentrations and chemical species were measured in three deep sea hydrothermal vent worms (Ridgeia piscesae, Paralvinella sulfincola and Paralvinella palmiformis ) from the Juan de Fuca Ridge in the Northwest pacific. R. piscesae has similar arsenic concentrations (3.8–35 µg g−1) to shallow water polychaetes while P. sulfincola and P. palmiformis have significantly higher arsenic concentrations (420–1417 and 125–321 µg g−1 respectively). R. piscesae contains appreciable quantities of inorganic arsenic (36±14%), monomethyl arsenic (2±2%), dimethyl arsenic (34±21%), an unknown methyl arsenical (7±16%), OSO3-arsenosugar (5±9%), \TETRA\ (4±5%), ThioPO4/ThioDMAE (1±2%) and an unknown thio-arsenical (12±14%). These results suggests that host and symbionts are either involved in the methylation of arsenic, or are bathed in fluids enriched in methylated arsenic as a result of free-living microbial activity. The host carrying out methylation, however, cannot be ruled out. In contrast, 96–97% of the arsenic in P. sulfincola and P. palmiformis is inorganic arsenic, likely the result of arsenic precipitation within and upon the mucus they ingest while feeding. While all worms have oxo- and thio arsenosugars (2–30%), Paralvinella also have small amounts of arsenobetaine (<0.001–0.21%). The presence of arsenosugars, arsenobetaine and other minor arsenic species in the absence of photosynthesising algae/bacteria indicates that they may be formed by vent animals in the absence of sunlight, but at this time their formation cannot be explained.
Girguis P. Microbial ecology: Here, there and everywhere. Nature Microbiology. 2016;1 :16123 - . Publisher's Version
Meier DV, Bach W, Girguis PR, Gruber-Vodicka HR, Reeves EP, Richter M, Vidoudez C, Amann R, Meyerdierks A. Heterotrophic Proteobacteria in the vicinity of diffuse hydrothermal venting. Environmental Microbiology. 2016 :n/a–n/a. Publisher's VersionAbstract
Deep-sea hydrothermal vents are highly dynamic habitats characterized by steep temperature and chemical gradients. The oxidation of reduced compounds dissolved in the venting fluids fuels primary production providing the basis for extensive life. Until recently studies of microbial vent communities have focused primarily on chemolithoautotrophic organisms. In our study, we targeted the change of microbial community compositions along mixing gradients, focusing on distribution and capabilities of heterotrophic microorganisms. Samples were retrieved from different venting areas within the Menez Gwen hydrothermal field, taken along mixing gradients, including diffuse fluid discharge points, their immediate surroundings and the buoyant parts of hydrothermal plumes. High throughput 16S rRNA gene amplicon sequencing, fluorescence in situ hybridization, and targeted metagenome analysis were combined with geochemical analyses. Close to diffuse venting orifices dominated by chemolithoautotrophic Epsilonproteobacteria, in areas where environmental conditions still supported chemolithoautotrophic processes, we detected microbial communities enriched for versatile heterotrophic Alpha- and Gammaproteobacteria. The potential for alkane degradation could be shown for several genera and yet uncultured clades. We propose that hotspots of chemolithoautotrophic life support a ‘belt’ of heterotrophic bacteria significantly different from the dominating oligotrophic microbiota of the deep sea.
Schrader PS, Reimers CE, Girguis P, Delaney J, Doolan C, Wolf M, Green D. Independent Benthic Microbial Fuel Cells Powering Sensors and Acoustic Communications with the MARS Underwater Observatory. Journal of Atmospheric and Oceanic Technology. 2016;33 (3) :607-617. Publisher's VersionAbstract
AbstractMost oceanographic instruments on the seafloor have no connections with the surface and therefore have to run on batteries and store data until recovery. To demonstrate a developing technology, sensors and acoustic modems were powered with energy harvested from the seafloor, and data were relayed acoustically in near–real time to the Monterey Accelerated Research System (MARS) observatory in Monterey Bay, California, and to surface research vessels. MARS is a cabled observatory in deep water ( 890 m) at the edge of Monterey Canyon. An acoustic modem was attached to the MARS node and configured to send out commands to, and relay data received from, remote modems. Two benthic microbial fuel cells (BMFCs) positioned approximately 0.5 km away from MARS supplied power to the remote modems and sensors. At their peak performance, these BMFCs produced continuous power densities of  35 mW m−2 (footprint area). The modems utilized in this study contained an integrated power management platform (PMP) designed to manage and store the electrical energy generated by each BMFC and to record BMFC performance parameters and sensor data on an hourly basis. Temperature and either oxygen or conductivity sensors were chosen because of their common use and environmental relevance. Acoustically transmitted data records show that the BMFCs renewed energy stores and that the oceanographic sensors measured dissolved oxygen, temperature, and conductivity reliably throughout the operational life of each BMFC system ( 6 months). These systems remained in place for more than 12 months.
Padilla CC, Bristow LA, Sarode N, Garcia-Robledo E, Gomez Ramirez E, Benson CR, Bourbonnais A, Altabet MA, Girguis PR, Thamdrup B, et al. NC10 bacteria in marine oxygen minimum zones. ISME J. 2016;10 (8) :2067 - 2071. Publisher's VersionAbstract
Bacteria of the NC10 phylum link anaerobic methane oxidation to nitrite denitrification through a unique O2-producing intra-aerobic methanotrophy pathway. A niche for NC10 in the pelagic ocean has not been confirmed. We show that NC10 bacteria are present and transcriptionally active in oceanic oxygen minimum zones (OMZs) off northern Mexico and Costa Rica. NC10 16S rRNA genes were detected at all sites, peaking in abundance in the anoxic zone with elevated nitrite and methane concentrations. Phylogenetic analysis of particulate methane monooxygenase genes further confirmed the presence of NC10. rRNA and mRNA transcripts assignable to NC10 peaked within the OMZ and included genes of the putative nitrite-dependent intra-aerobic pathway, with high representation of transcripts containing the unique motif structure of the nitric oxide (NO) reductase of NC10 bacteria, hypothesized to participate in O2-producing NO dismutation. These findings confirm pelagic OMZs as a niche for NC10, suggesting a role for this group in OMZ nitrogen, methane and oxygen cycling.
Seston SL, Beinart RA, Sarode N, Shockey AC, Ranjan P, Ganesh S, Girguis PR, Stewart FJ. Metatranscriptional Response of Chemoautotrophic Ifremeria nautilei Endosymbionts to Differing Sulfur Regimes. Frontiers in Microbiology. 2016;7 :1074. Publisher's VersionAbstract
Endosymbioses between animals and chemoautotrophic bacteria are ubiquitous at hydrothermal vents. These environments are distinguished by high physico-chemical variability, yet we know little about how these symbioses respond to environmental fluctuations. We therefore examined how the γ-proteobacterial symbionts of the vent snail Ifremeria nautilei respond to changes in sulfur geochemistry. Via shipboard high-pressure incubations, we subjected snails to 105 μM hydrogen sulfide (LS), 350 μM hydrogen sulfide (HS), 300 μM thiosulfate (TS) and seawater without any added inorganic electron donor (ND). While transcript levels of sulfur oxidation genes were largely consistent across treatments, HS and TS treatments stimulated genes for denitrification, nitrogen assimilation, and CO(2) fixation, coincident with previously reported enhanced rates of inorganic carbon incorporation and sulfur oxidation in these treatments. Transcripts for genes mediating oxidative damage were enriched in the ND and LS treatments, potentially due to a reduction in O(2) scavenging when electron donors were scarce. Oxidative TCA cycle gene transcripts were also more abundant in ND and LS treatments, suggesting that I. nautilei symbionts may be mixotrophic when inorganic electron donors are limiting. These data reveal the extent to which I. nautilei symbionts respond to changes in sulfur concentration and species, and, interpreted alongside coupled biochemical metabolic rates, identify gene targets whose expression patterns may be predictive of holobiont physiology in environmental samples.
Picard A, Gartman A, Girguis PR. What Do We Really Know about the Role of Microorganisms in Iron Sulfide Mineral Formation?. Frontiers in Earth Science. 2016;4 :68. Publisher's VersionAbstract
Iron sulfide mineralization in low-temperature systems is a result of biotic and abiotic processes, though the delineation between these two modes of formation is not always straightforward. Here we review the role of microorganisms in the precipitation of extracellular iron sulfide minerals. We summarize the evidence that links sulfur-metabolizing microorganisms and sulfide minerals in nature and we present a critical overview of laboratory-based studies of the nucleation and growth of iron sulfide minerals in microbial cultures. We discuss whether biologically derived minerals are distinguishable from abiotic minerals, possessing attributes that are uniquely diagnostic of biomineralization. These inquiries have revealed the need for additional thorough, mechanistic and high-resolution studies to understand microbially mediated formation of a variety of sulfide minerals across a range of natural environments.

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