Person: Girguis, Peter
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Girguis
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Girguis, Peter
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Publication Baleen whales host a unique gut microbiome with similarities to both carnivores and herbivores(Nature Pub. Group, 2015) Sanders, Jon G.; Beichman, Annabel C.; Roman, Joe; Scott, Jarrod J.; Emerson, David; Mccarthy, James; Girguis, PeterMammals host gut microbiomes of immense physiological consequence, but the determinants of diversity in these communities remain poorly understood. Diet appears to be the dominant factor, but host phylogeny also seems to be an important, if unpredictable, correlate. Here we show that baleen whales, which prey on animals (fish and crustaceans), harbor unique gut microbiomes with surprising parallels in functional capacity and higher level taxonomy to those of terrestrial herbivores. These similarities likely reflect a shared role for fermentative metabolisms despite a shift in primary carbon sources from plant-derived to animal-derived polysaccharides, such as chitin. In contrast, protein catabolism and essential amino acid synthesis pathways in baleen whale microbiomes more closely resemble those of terrestrial carnivores. Our results demonstrate that functional attributes of the microbiome can vary independently even given an animal-derived diet, illustrating how diet and evolutionary history combine to shape microbial diversity in the mammalian gut.Publication Carbon fixation by basalt-hosted microbial communities(Frontiers Media S.A., 2015) Orcutt, Beth N.; Sylvan, Jason B.; Rogers, Daniel R.; Delaney, Jennifer; Lee, Raymond W.; Girguis, PeterOceanic crust is a massive potential habitat for microbial life on Earth, yet our understanding of this ecosystem is limited due to difficulty in access. In particular, measurements of rates of microbial activity are sparse. We used stable carbon isotope incubations of crustal samples, coupled with functional gene analyses, to examine the potential for carbon fixation on oceanic crust. Both seafloor-exposed and subseafloor basalts were recovered from different mid-ocean ridge and hot spot environments (i.e., the Juan de Fuca Ridge, the Mid-Atlantic Ridge, and the Loihi Seamount) and incubated with 13C-labeled bicarbonate. Seafloor-exposed basalts revealed incorporation of 13C-label into organic matter over time, though the degree of incorporation was heterogeneous. The incorporation of 13C into biomass was inconclusive in subseafloor basalts. Translating these measurements into potential rates of carbon fixation indicated that 0.1–10 nmol C g-1rock d-1 could be fixed by seafloor-exposed rocks. When scaled to the global production of oceanic crust, this suggests carbon fixation rates of 109–1012 g C year-1, which matches earlier predictions based on thermodynamic calculations. Functional gene analyses indicate that the Calvin cycle is likely the dominant biochemical mechanism for carbon fixation in basalt-hosted biofilms, although the reductive acetyl-CoA pathway and reverse TCA cycle likely play some role in net carbon fixation. These results provide empirical evidence for autotrophy in oceanic crust, suggesting that basalt-hosted autotrophy could be a significant contributor of organic matter in this remote and vast environment.Publication Characterizing the distribution and rates of microbial sulfate reduction at Middle Valley hydrothermal vents(Nature Publishing Group, 2013) Frank, Kiana L; Rogers, Daniel R.; Olins, Heather; Vidoudez, Charles; Girguis, PeterFew studies have directly measured sulfate reduction at hydrothermal vents, and relatively little is known about how environmental or ecological factors influence rates of sulfate reduction in vent environments. A better understanding of microbially mediated sulfate reduction in hydrothermal vent ecosystems may be achieved by integrating ecological and geochemical data with metabolic rate measurements. Here we present rates of microbially mediated sulfate reduction from three distinct hydrothermal vents in the Middle Valley vent field along the Juan de Fuca Ridge, as well as assessments of bacterial and archaeal diversity, estimates of total biomass and the abundance of functional genes related to sulfate reduction, and in situ geochemistry. Maximum rates of sulfate reduction occurred at 90 °C in all three deposits. Pyrosequencing and functional gene abundance data revealed differences in both biomass and community composition among sites, including differences in the abundance of known sulfate-reducing bacteria. The abundance of sequences for Thermodesulfovibro-like organisms and higher sulfate reduction rates at elevated temperatures suggests that Thermodesulfovibro-like organisms may have a role in sulfate reduction in warmer environments. The rates of sulfate reduction presented here suggest that—within anaerobic niches of hydrothermal deposits—heterotrophic sulfate reduction may be quite common and might contribute substantially to secondary productivity, underscoring the potential role of this process in both sulfur and carbon cycling at vents.Publication Anaerobic Methane Oxidation in Metalliferous Hydrothermal Sediments: Influence on Carbon Flux and Decoupling from Sulfate Reduction(Wiley-Blackwell, 2012) Wankel, Scott D.; Adams, Melissa Marie; Johnston, David; Hansel, Colleen; Joye, Samantha B.; Girguis, PeterThe anaerobic oxidation of methane (AOM) is a globally significant sink that regulates methane flux from sediments into the oceans and atmosphere. Here we examine mesophilic to thermophilic AOM in hydrothermal sediments recovered from the Middle Valley vent field, on the Juan de Fuca Ridge. Using continuous-flow sediment bioreactors and batch incubations, we characterized (i) the degree to which AOM contributes to net dissolved inorganic carbon flux, (ii) AOM and sulfate reduction (SR) rates as a function of temperature and (iii) the distribution and density of known anaerobic methanotrophs (ANMEs). In sediment bioreactors, inorganic carbon stable isotope mass balances results indicated that AOM accounted for between 16% and 86% of the inorganic carbon produced, underscoring the role of AOM in governing inorganic carbon flux from these sediments. At 90°C, AOM occurred in the absence of SR, demonstrating a striking decoupling of AOM from SR. An abundance of Fe(III)-bearing minerals resembling mixed valent Fe oxides, such as green rust, suggests the potential for a coupling of AOM to Fe(III) reduction in these metalliferous sediments. While SR bacteria were only observed in cooler temperature sediments, ANMEs allied to ANME-1 ribotypes, including a putative ANME-1c group, were found across all temperature regimes and represented a substantial proportion of the archaeal community. In concert, these results extend and reshape our understanding of the nature of high temperature methane biogeochemistry, providing insight into the physiology and ecology of thermophilic anaerobic methanotrophy and suggesting that AOM may play a central role in regulating biological dissolved inorganic carbon fluxes to the deep ocean from the organic-poor, metalliferous sediments of the global mid-ocean ridge hydrothermal vent system.Publication Oxygen, Ecology, and the Cambrian Radiation of Animals(Proceedings of the National Academy of Sciences, 2013) Sperling, Erik A.; Frieder, Christina A.; Raman, Akkur V.; Girguis, Peter; Levin, Lisa A.; Knoll, AndrewThe Proterozoic-Cambrian transition records the appearance of essentially all animal body plans (phyla), yet to date no single hypothesis adequately explains both the timing of the event and the evident increase in diversity and disparity. Ecological triggers focused on escalatory predator–prey “arms races” can explain the evolutionary pattern but not its timing, whereas environmental triggers, particularly ocean/atmosphere oxygenation, do the reverse. Using modern oxygen minimum zones as an analog for Proterozoic oceans, we explore the effect of low oxygen levels on the feeding ecology of polychaetes, the dominant macrofaunal animals in deep-sea sediments. Here we show that low oxygen is clearly linked to low proportions of carnivores in a community and low diversity of carnivorous taxa, whereas higher oxygen levels support more complex food webs. The recognition of a physiological control on carnivory therefore links environmental triggers and ecological drivers, providing an integrated explanation for both the pattern and timing of Cambrian animal radiation.Publication Geomicrobiological linkages between short-chain alkane consumption and sulfate reduction rates in seep sediments(Frontiers Media S.A., 2013) Bose, Arpita; Rogers, Daniel R.; Adams, Melissa Marie; Joye, Samantha B.; Girguis, PeterMarine hydrocarbon seeps are ecosystems that are rich in methane, and, in some cases, short-chain (C2–C5) and longer alkanes. C2–C4 alkanes such as ethane, propane, and butane can be significant components of seeping fluids. Some sulfate-reducing microbes oxidize short-chain alkanes anaerobically, and may play an important role in both the competition for sulfate and the local carbon budget. To better understand the anaerobic oxidation of short-chain n-alkanes coupled with sulfate-reduction, hydrocarbon-rich sediments from the Gulf of Mexico (GoM) were amended with artificial, sulfate-replete seawater and one of four n-alkanes (C1–C4) then incubated under strict anaerobic conditions. Measured rates of alkane oxidation and sulfate reduction closely follow stoichiometric predictions that assume the complete oxidation of alkanes to CO2 (though other sinks for alkane carbon likely exist). Changes in the δ13C of all the alkanes in the reactors show enrichment over the course of the incubation, with the C3 and C4 incubations showing the greatest enrichment (4.4 and 4.5‰, respectively). The concurrent depletion in the δ13C of dissolved inorganic carbon (DIC) implies a transfer of carbon from the alkane to the DIC pool (−3.5 and −6.7‰ for C3 and C4 incubations, respectively). Microbial community analyses reveal that certain members of the class Deltaproteobacteria are selectively enriched as the incubations degrade C1–C4 alkanes. Phylogenetic analyses indicate that distinct phylotypes are enriched in the ethane reactors, while phylotypes in the propane and butane reactors align with previously identified C3–C4 alkane-oxidizing sulfate-reducers. These data further constrain the potential influence of alkane oxidation on sulfate reduction rates (SRRs) in cold hydrocarbon-rich sediments, provide insight into their contribution to local carbon cycling, and illustrate the extent to which short-chain alkanes can serve as electron donors and govern microbial community composition and density.Publication Quantitative population dynamics of microbial communities in plankton-fed microbial fuel cells(Springer Nature, 2009) White, Helen K; Reimers, Clare E; Cordes, Erik E; Dilly, Geoffrey F; Girguis, PeterThis study examines changes in diversity and abundance of bacteria recovered from the anodes of microbial fuel cells (MFCs) in relation to anode potential, power production and geochemistry. MFCs were batch-fed with plankton, and two systems were maintained at different potentials whereas one was at open circuit for 56.8 days. Bacterial phylogenetic diversity during peak power was assessed from 16S rDNA clone libraries. Throughout the experiment, microbial community structure was examined using terminal restriction fragment length polymorphism. Changes in cell density of key phylotypes, including representatives of δ-, ε-, γ-proteobacteria and Flavobacterium-Cytophaga-Bacteroides, were enumerated by quantitative PCR. Marked differences in phylogenetic diversity were observed during peak power versus the final time point, and changes in microbial community structure were strongly correlated to dissolved organic carbon and ammonium concentrations within the anode chambers. Community structure was notably different between the MFCs at different anode potentials during the onset of peak power. At the final time point, however, the anode-hosted communities in all MFCs were similar. These data demonstrate that differences in growth, succession and population dynamics of key phylotypes were due to anode potential, which may relate to their ability to exploit the anode as an electron acceptor. The geochemical milieu, however, governs overall community diversity and structure. These differences reflect the physiological capacity of specific phylotypes to catabolize plankton-derived organic matter and exploit the anode of an MFC for their metabolism directly or indirectly through syntrophy.Publication Harnessing energy from marine productivity using bioelectrochemical systems(Elsevier BV, 2010) Girguis, Peter; Nielsen, Mark E; Figueroa, IsraelOver the past decade, studies have shown that devices called microbial fuel cells (MFCs) can harness electricity from microbially mediated degradation of organic carbon, in both lab cultures and natural environments. Other studies have shown that MFCs can harness power from coastal and deep ocean sediments, as well as from plankton, without any fuel supplementation or microbial inoculation. The fuel for these systems is organic matter resulting from oceanic primary productivity. Models suggest that MFCs may operate for decades on endogenous organic carbon. In light of their capacity to generate power in natural milieus by tapping into biogeochemical cycles, MFCs may one day provide an efficient means of generating power (or high value biofuels) directly from marine productivity.Publication Links from Mantle to Microbe at the Lau Integrated Study Site: Insights from a Back-Arc Spreading Center(The Oceanography Society, 2012) Tivey, Margaret; Becker, Erin; Beinart, Roxanne; Fisher, Charles; Girguis, Peter; Langmuir, Charles; Michael, Peter; Reysenbach, Anna-LouiseThe Lau Integrated Study Site (ISS) has provided unique opportunities for study of ridge processes because of its back-arc setting in the southwestern Pacific. Its location allows study of a biogeographical province distinct from those of eastern Pacific and mid-Atlantic ridges, and crustal compositions along the ridge lie outside the range of mid-ocean ridge crustal compositions. The Lau ISS is located above a subduction zone, at an oblique angle. The underlying mantle receives water and other elements derived from the downgoing lithospheric slab, with an increase in slab influence from north to south. Water lowers the mantle melting temperature and leads to greater melt production where the water flux is greater, and to distinctive regional-scale gradients along the ridge. There are deeper faulted axial valleys with basaltic volcanism in the north and inflated axial highs with andesites in the south. Differences in igneous rock composition and release of magmatic volatiles affect compositions of vent fluids and deposits. Differences in vent fluid compositions and small-scale diffuse-flow regimes correlate with regional-scale patterns in microbial and megafaunal distributions. The interdisciplinary research effort at the Lau ISS has successfully identified linkages between subsurface processes and deep-sea biological communities, from mantle to microbe to megafauna.Publication Electron Uptake by Iron-Oxidizing Phototrophic Bacteria(Nature Publishing Group, 2014) Bose, Arpita; Gardel, Emily Jeanette; Vidoudez, Charles; Parra, Erika; Girguis, PeterOxidation–reduction reactions underlie energy generation in nearly all life forms. Although most organisms use soluble oxidants and reductants, some microbes can access solid-phase materials as electron-acceptors or -donors via extracellular electron transfer. Many studies have focused on the reduction of solid-phase oxidants. Far less is known about electron uptake via microbial extracellular electron transfer, and almost nothing is known about the associated mechanisms. Here we show that the iron-oxidizing photoautotroph Rhodopseudomonas palustris TIE-1 accepts electrons from a poised electrode, with carbon dioxide as the sole carbon source/electron acceptor. Both electron uptake and ruBisCo form I expression are stimulated by light. Electron uptake also occurs in the dark, uncoupled from photosynthesis. Notably, the pioABC operon, which encodes a protein system essential for photoautotrophic growth by ferrous iron oxidation, influences electron uptake. These data reveal a previously unknown metabolic versatility of photoferrotrophs to use extracellular electron transfer for electron uptake.