Publications

2014
Picard A, Gartman A, Clarke DR, Girguis PR. Sulfate Reduction and Sulfide Biomineralization by Deep-Sea Hydrothermal Vent Microorganisms, in AGU Fall Meeting Abstracts. Vol 2014. ; 2014 :B13A–0164.
Liao L, Wankel SD, Wu M, Cavanaugh CM, Girguis PR. Characterizing the plasticity of nitrogen metabolism by the host and symbionts of the hydrothermal vent chemoautotrophic symbioses Ridgeia piscesae. Molecular Ecology. 2014;23 :1544-1557.Abstract

Chemoautotrophic symbionts of deep sea hydrothermal vent tubeworms are known to provide their hosts with all their primary nutrition. While studies have examined how chemoautotrophic symbionts provide the association with nitrogen, fewer have examined if symbiont nitrogen metabolism varies as a function of environmental conditions. Ridgeia piscesae tubeworms flourish at Northeastern Pacific vents, occupy a range of microhabitats, and exhibit a high degree of morphological plasticity [e.g. long-skinny (LS) and short-fat (SF) phenotypes] that may relate to environmental conditions. This plasticity affords an opportunity to examine whether symbiont nitrogen metabolism varies among host phenotypes. LS and SF R.piscesae were recovered from the Axial and Main Endeavour Field hydrothermal vents. Nitrate and ammonium were quantified in Ridgeia blood, and the expression of key nitrogen metabolism genes, as well as stable nitrogen isotope ratios, was quantified in host branchial plume and symbiont-containing tissues. Nitrate and ammonium were abundant in the blood of both phenotypes though environmental ammonium concentrations were, paradoxically, lowest among individuals with the highest blood ammonium. Assimilatory nitrate reductase transcripts were always below detection, though in both LS and SF R.piscesae symbionts, we observed elevated expression of dissimilatory nitrate reductase genes, as well as symbiont and host ammonium assimilation genes. Site-specific differences in expression, along with tissue stable isotope analyses, suggest that LS and SF Ridgeia symbionts are engaged in both dissimilatory nitrate reduction and ammonia assimilation to varying degrees. As such, it appears that environmental conditions -not host phenotype-primarily dictates symbiont nitrogen metabolism.

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Bose A, Gardel EJ, Vidoudez C, Parra EA, Girguis PR. Electron uptake by iron-oxidizing phototrophic bacteria. Nature Communications. 2014;5 :1-7.Abstract

Oxidation-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.

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Beinart RA, Nyholm SV, Dubilier N, Girguis PR. Intracellular Oceanospirillales inhabit the gills of the hydrothermal vent snail Alviniconcha with chemosynthetic, gamma-Proteobacterial symbionts. Environmental Microbiology Reports. 2014;6 :656-664.Abstract

Associations between bacteria from the -Proteobacterial order Oceanospirillales and marine invertebrates are quite common. Members of the Oceanospirillales exhibit a diversity of interactions with their various hosts, ranging from the catabolism of complex compounds that benefit host growth to attacking and bursting host nuclei. Here, we describe the association between a novel Oceanospirillales phylotype and the hydrothermal vent snail Alviniconcha. Alviniconcha typically harbour chemoautotrophic - or epsilon-Proteobacterial symbionts inside their gill cells. Via fluorescence in situ hybridization and transmission electron microscopy, we observed an Oceanospirillales phylotype (named AOP for AlviniconchaOceanospirillales phylotype') in membrane-bound vacuoles that were separate from the known - or epsilon-Proteobacterial symbionts. Using quantitative polymerase chain reaction, we surveyed 181 Alviniconcha hosting -Proteobacterial symbionts and 102 hosting epsilon-Proteobacterial symbionts, and found that the population size of AOP was always minor relative to the canonical symbionts (median 0.53% of the total quantified 16S rRNA genes). Additionally, we detected AOP more frequently in Alviniconcha hosting -Proteobacterial symbionts than in those hosting epsilon-Proteobacterial symbionts (96% and 5% of individuals respectively). The high incidence of AOP in -Proteobacteria hosting Alviniconcha implies that it could play a significant ecological role either as a host parasite or as an additional symbiont with unknown physiological capacities.

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Sperling EA, Frieder CA, Raman AV, Girguis PR, Levin LA, Knoll AH. Oxygen, ecology, and the Cambrian radiation of animals. Integrative and Comparative Biology. 2014;54 :E198-E198.
2013
Adams MM, Hoarfrost AL, Bose A, Joye SB, Girguis PR. Anaerobic oxidation of short-chain alkanes in hydrothermal sediments: potential influences on sulfur cycling and microbial diversity. Frontiers in Microbiology. 2013;4 :110.
Olins HC, Rogers DR, Frank KL, Vidoudez C, Girguis PR. Assessing the influence of physical, geochemical and biological factors on anaerobic microbial primary productivity within hydrothermal vent chimneys. Geobiology. 2013;11 (3) :279–293.
Ussler III W, Preston C, Tavormina P, Pargett D, Jensen S, Roman B, Marin III R, Shah SR, Girguis PR, Birch JM, et al. Autonomous application of quantitative PCR in the deep sea: in situ surveys of aerobic methanotrophs using the deep-sea environmental sample processor. Environmental science & technology. 2013;47 (16) :9339–9346.
Girguis P, Reimers CE. Biochemical systems for sulfur and carbon sequestration. 2013.
Adams MM, Biddle J, Girguis PR. Biogeography and diversity of methane and sulfur-cycling ecotypes in deep subsurface sediments, in AGU Fall Meeting Abstracts. Vol 2013. ; 2013 :B13C–0484.
Robidart J, Callister SJ, Song P, Nicora CD, Wheat CG, Girguis PR. Characterizing microbial community and geochemical dynamics at hydrothermal vents using osmotically driven continuous fluid samplers. Environmental science & technology. 2013;47 (9) :4399–4407.
Frank KL, Rogers DR, Olins HC, Vidoudez C, Girguis PR. Characterizing the distribution and rates of microbial sulfate reduction at Middle Valley hydrothermal vents. The ISME journal. 2013;7 (7) :1391–1401.
Wankel SD, Huang Y-wen, Gupta M, Provencal R, Leen BJ, Fahrland A, Vidoudez C, Girguis PR. Characterizing the distribution of methane sources and cycling in the deep sea via in situ stable isotope analysis. Environmental science & technology. 2013;47 (3) :1478–1486.
Pargett DM, Jensen SD, Roman BA, Preston CM, Ussler W, Girguis PR, Marin R, Birch JM, Scholin CA. Deep water instrument for microbial identification, quantification, and archiving, in 2013 OCEANS-San Diego. IEEE ; 2013 :1–6.
Bose A, Rogers DR, Adams MM, Joye SB, Girguis PR. Geomicrobiological linkages between short-chain alkane consumption and sulfate reduction rates in seep sediments. Frontiers in microbiology. 2013;4 :386.
Perner M, Gonnella G, Hourdez S, Böhnke S, Kurtz S, Girguis P. In situ chemistry and microbial community compositions in five deep-sea hydrothermal fluid samples from I rina II in the L ogatchev field. Environmental Microbiology. 2013;15 (5) :1551–1560.
Sylvan JB, Sia TY, Haddad AG, Briscoe LJ, Toner BM, Girguis PR, Edwards KJ. Low temperature geomicrobiology follows host rock composition along a geochemical gradient in Lau Basin. Frontiers in Microbiology. 2013;4 :61.
Sanders JG, Beinart RA, Stewart FJ, Delong EF, Girguis PR. Metatranscriptomics reveal differences in in situ energy and nitrogen metabolism among hydrothermal vent snail symbionts. The ISME journal. 2013;7 (8) :1556–1567.
Girguis PR, Jaekel U, Dittmar T, Meyer JL, Glazer BT, Huber JA. Microbial transformations of carbon in crustal aquifer fluids at North Pond, Mid-Atlantic Ridge, in AGU Fall Meeting Abstracts. Vol 2013. ; 2013 :B23G–02.
Sperling EA, Frieder CA, Raman AV, Girguis PR, Levin LA, Knoll AH. Oxygen, ecology, and the Cambrian radiation of animals. Proceedings of the National Academy of Sciences. 2013;110 (33) :13446–13451.

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