Professional Education


  • Doctor of Philosophy, University of Georgia (2014)

Stanford Advisors


All Publications


  • Light and temperature control the seasonal distribution of thaumarchaeota in the South Atlantic bight ISME JOURNAL Liu, Q., Tolar, B. B., Ross, M. J., Cheek, J. B., Sweeney, C. M., Wallsgrove, N. J., Popp, B. N., Hollibaugh, J. T. 2018; 12 (6): 1473–85

    Abstract

    Mid-summer peaks in the abundance of Thaumarchaeota and nitrite concentration observed on the Georgia, USA, coast could result from in situ activity or advection of populations from another source. We collected data on the distribution of Thaumarchaeota, ammonia-oxidizing betaproteobacteria (AOB), Nitrospina, environmental variables and rates of ammonia oxidation during six cruises in the South Atlantic Bight (SAB) from April to November 2014. These data were used to examine seasonality of nitrification in offshore waters and to test the hypothesis that the bloom was localized to inshore waters. The abundance of Thaumarchaeota marker genes (16S rRNA and amoA) increased at inshore and nearshore stations starting in July and peaked in August at >107 copies L-1. The bloom did not extend onto the mid-shelf, where Thaumarchaeota genes ranged from 103 to 105 copies L-1. Ammonia oxidation rates (AO) were highest at inshore stations during summer (to 840 nmol L-1 d-1) and were always at the limit of detection at mid-shelf stations. Nitrite concentrations were correlated with AO (R = 0.94) and were never elevated at mid-shelf stations. Gene sequences from samples collected at mid-shelf stations generated using Archaea 16S rRNA primers were dominated by Euryarchaeota; sequences from inshore and nearshore stations were dominated by Thaumarchaeota. Thaumarchaeota were also abundant at depth at the shelf-break; however, this population was phylogenetically distinct from the inshore/nearshore population. Our analysis shows that the bloom is confined to inshore waters during summer and suggests that Thaumarchaeota distributions in the SAB are controlled primarily by photoinhibition and secondarily by water temperature.

    View details for DOI 10.1038/s41396-018-0066-4

    View details for Web of Science ID 000432357500007

    View details for PubMedID 29445129

    View details for PubMedCentralID PMC5956005

  • Cryo Electron Tomography and Reaction-Diffusion Simulations Reveal a Molecular and Evolutionary Basis for Charged Archaeal Surface Layer Proteins Li, P., Herrmann, J. R., Poitevin, F. B., Ramdasi, R., Tolar, B. B., Barger, J., Stahl, D., Jensen, G., Wakatsuki, S., van den Bedem, H. CELL PRESS. 2018: 495A
  • Oxidation of urea-derived nitrogen by thaumarchaeota-dominated marine nitrifying communities ENVIRONMENTAL MICROBIOLOGY Tolar, B. B., Wallsgrove, N. J., Popp, B. N., Hollibaugh, J. T. 2017; 19 (12): 4838–50

    Abstract

    Urea nitrogen has been proposed to contribute significantly to nitrification by marine thaumarchaeotes. These inferences are based on distributions of thaumarchaeote urease genes rather than activity measurements. We found that ammonia oxidation rates were always higher than oxidation rates of urea-derived N in samples from coastal Georgia, USA (means ± SEM: 382 ± 35 versus 73 ± 24 nmol L-1  d-1 , Mann-Whitney U-test p < 0.0001), and the South Atlantic Bight (20 ± 8.8 versus 2.2 ± 1.7 nmol L-1  d-1 , p = 0.026) but not the Gulf of Alaska (8.8 ± 4.0 versus 1.5 ± 0.6, p > 0.05). Urea-derived N was relatively more important in samples from Antarctic continental shelf waters, though the difference was not statistically significant (19.4 ± 4.8 versus 12.0 ± 2.7 nmol L-1  d-1 , p > 0.05). We found only weak correlations between oxidation rates of urea-derived N and the abundance or transcription of putative Thaumarchaeota ureC genes. Dependence on urea-derived N does not appear to be directly related to pH or ammonium concentrations. Competition experiments and release of 15 NH3 suggest that urea is hydrolyzed to ammonia intracellularly, then a portion is lost to the dissolved pool. The contribution of urea-derived N to nitrification appears to be minor in temperate coastal waters, but may represent a significant portion of the nitrification flux in Antarctic coastal waters.

    View details for DOI 10.1111/1462-2920.13457

    View details for Web of Science ID 000418352800005

    View details for PubMedID 27422798

  • Realizing the potential of trait-based aquatic ecology: New tools and collaborative approaches LIMNOLOGY AND OCEANOGRAPHY Kremer, C. T., Williams, A. K., Finiguerra, M., Fong, A. A., Kellerman, A., Paver, S. F., Tolar, B. B., Toscano, B. J. 2017; 62 (1): 253-271

    View details for DOI 10.1002/lno.10392

    View details for Web of Science ID 000393804600017

  • Integrated structural biology and molecular ecology of N-cycling enzymes from ammonia-oxidizing archaea. Environmental microbiology reports Tolar, B. B., Herrmann, J., Bargar, J. R., van den Bedem, H., Wakatsuki, S., Francis, C. A. 2017; 9 (5): 484–91

    Abstract

    Knowledge of the molecular ecology and environmental determinants of ammonia-oxidizing organisms is critical to understanding and predicting the global nitrogen (N) and carbon cycles, but an incomplete biochemical picture hinders in vitro studies of N-cycling enzymes. Although an integrative structural and dynamic characterization at the atomic scale would advance our understanding of function tremendously, structural knowledge of key N-cycling enzymes from ecologically relevant ammonia oxidizers is unfortunately extremely limited. Here, we discuss the challenges and opportunities for examining the ecology of ammonia-oxidizing organisms, particularly uncultivated Thaumarchaeota, through (meta)genome-driven structural biology of the enzymes ammonia monooxygenase (AMO) and nitrite reductase (NirK).

    View details for DOI 10.1111/1758-2229.12567

    View details for PubMedID 28677304

  • Contribution of ammonia oxidation to chemoautotrophy in Antarctic coastal waters ISME JOURNAL Tolar, B. B., Ross, M. J., Wallsgrove, N. J., Liu, Q., Aluwihare, L. I., Popp, B. N., Hollibaugh, J. T. 2016; 10 (11): 2605-2619

    Abstract

    There are few measurements of nitrification in polar regions, yet geochemical evidence suggests that it is significant, and chemoautotrophy supported by nitrification has been suggested as an important contribution to prokaryotic production during the polar winter. This study reports seasonal ammonia oxidation (AO) rates, gene and transcript abundance in continental shelf waters west of the Antarctic Peninsula, where Thaumarchaeota strongly dominate populations of ammonia-oxidizing organisms. Higher AO rates were observed in the late winter surface mixed layer compared with the same water mass sampled during summer (mean±s.e.: 62±16 versus 13±2.8 nm per day, t-test P<0.0005). AO rates in the circumpolar deep water did not differ between seasons (21±5.7 versus 24±6.6 nm per day; P=0.83), despite 5- to 20-fold greater Thaumarchaeota abundance during summer. AO rates correlated with concentrations of Archaea ammonia monooxygenase (amoA) genes during summer, but not with concentrations of Archaea amoA transcripts, or with ratios of Archaea amoA transcripts per gene, or with concentrations of Betaproteobacterial amoA genes or transcripts. The AO rates we report (<0.1-220 nm per day) are ~10-fold greater than reported previously for Antarctic waters and suggest that inclusion of Antarctic coastal waters in global estimates of oceanic nitrification could increase global rate estimates by ~9%. Chemoautotrophic carbon fixation supported by AO was 3-6% of annualized phytoplankton primary production and production of Thaumarchaeota biomass supported by AO could account for ~9% of the bacterioplankton production measured in winter. Growth rates of thaumarchaeote populations inferred from AO rates averaged 0.3 per day and ranged from 0.01 to 2.1 per day.

    View details for DOI 10.1038/ismej.2016.61

    View details for Web of Science ID 000387035700005

    View details for PubMedID 27187795

    View details for PubMedCentralID PMC5113851