Bio


I am an aquatic microbiologist is interested in figuring out how microorganisms respond to environmental change and whether that determines "who" we find in oceans, estuaries, rivers, and lakes. My work focuses on seasonal dynamics of marine archaea (Thaumarchaeota) in Monterey Bay and floodplains in the western US, their role in the nitrogen cycle, and how these same organisms respond to stress in the laboratory. In addition to my research, I am passionate about mentoring students and participating in outreach programs to bring science to people of all ages, and am committed to making science more accessible to the public. I also work toward making STEM more diverse, equitable, and inclusive through mentoring and organizing programs among trainees.

Academic Appointments


Honors & Awards


  • Certificate of Outstanding Achievement in Mentoring, Stanford Earth (2019)
  • Research Review – Best Talk, Stanford Earth (2016)

Professional Education


  • Doctor of Philosophy, University of Georgia, Microbiology (2014)
  • Bachelor of Science, Louisiana State University, Microbiology (2008)

All Publications


  • ` Stability of Floodplain Subsurface Microbial Communities Through Seasonal Hydrological and Geochemical Cycles FRONTIERS IN EARTH SCIENCE Tolar, B. B., Boye, K., Bobb, C., Maher, K., Bargar, J. R., Francis, C. A. 2020; 8
  • Time series assessment of Thaumarchaeota ecotypes in Monterey Bay reveals the importance of water column position in predicting distribution-environment relationships Limnology and Oceanography Tolar, B. B., Reji, L., Smith, J. M., Blum, M., Pennington, J. T., Chavez, F. P., Francis, C. A. 2020

    View details for DOI 10.1002/LNO.11436

  • Depth-differentiation and seasonality of planktonic microbial assemblages in the Monterey Bay upwelling system Frontiers in Microbiology Reji, L., Tolar, B. B., Chavez, F. P., Francis, C. A. 2020

    View details for DOI 10.3389/fmicb.2020.01075

  • Coastal Ocean Metagenomes and Curated Metagenome-Assembled Genomes from Marsh Landing, Sapelo Island (Georgia, USA) MICROBIOLOGY RESOURCE ANNOUNCEMENTS Damashek, J., Edwardson, C. F., Tolar, B. B., Gifford, S. M., Moran, M., Hollibaugh, J. T. 2019; 8 (40)

    Abstract

    Microbes play a dominant role in the biogeochemistry of coastal waters, which receive organic matter from diverse sources. We present metagenomes and 45 metagenome-assembled genomes (MAGs) from Sapelo Island, Georgia, to further understand coastal microbial populations. Notably, four MAGs are archaea, with two Thaumarchaeota and two marine group II Euryarchaeota.

    View details for DOI 10.1128/MRA.00934-19

    View details for Web of Science ID 000489010100029

    View details for PubMedID 31582460

  • Depth distributions of Nitrite Reductase (nirK) Gene Variants Reveal Spatial Dynamics of Thaumarchaeal Ecotype Populations in Coastal Monterey Bay. Environmental microbiology Reji, L., Tolar, B. B., Smith, J. M., Chavez, F. P., Francis, C. A. 2019

    Abstract

    Ammonia-oxidizing archaea (AOA) of the phylum Thaumarchaeota are key players in nutrient cycling, yet large gaps remain in our understanding of their ecology and metabolism. Despite multiple lines of evidence pointing to a central role for copper-containing nitrite reductase (NirK) in AOA metabolism, the thaumarchaeal nirK gene is rarely studied in the environment. In this study, we examine the diversity of nirK in the marine pelagic environment, in light of previously described ecological patterns of pelagic thaumarchaeal populations. Phylogenetic analyses show that nirK better resolves diversification patterns of marine Thaumarchaeota, compared to the conventionally used marker gene amoA. Specifically, we demonstrate that the three major phylogenetic clusters of marine nirK correspond to the three 'ecotype' populations of pelagic Thaumarchaeota. In this context, we further examine the relative distributions of the three variant groups in metagenomes and metatranscriptomes representing two depth profiles in coastal Monterey Bay. Our results reveal that nirK effectively tracks the dynamics of thaumarchaeal ecotype populations, particularly finer-scale diversification patterns within major lineages. We also find evidence for multiple copies of nirK per genome in a fraction of thaumarchaeal cells in the water column, which must be taken into account when using it as a molecular marker. This article is protected by copyright. All rights reserved.

    View details for DOI 10.1111/1462-2920.14753

    View details for PubMedID 31330081

  • Differential co-occurrence relationships shaping ecotype diversification within Thaumarchaeota populations in the coastal ocean water column ISME JOURNAL Reji, L., Tolar, B. B., Smith, J. M., Chavez, F. P., Francis, C. A. 2019; 13 (5): 1144–58
  • Microbial oxidation of nitrogen supplied as selected organic nitrogen compounds in the South Atlantic Bight LIMNOLOGY AND OCEANOGRAPHY Damashek, J., Tolar, B. B., Liu, Q., Okotie-Oyekan, A. O., Wallsgrove, N. J., Popp, B. N., Hollibaugh, J. T. 2019; 64 (3): 982–95

    View details for DOI 10.1002/lno.11089

    View details for Web of Science ID 000467593600009

  • Differential co-occurrence relationships shaping ecotype diversification within Thaumarchaeota populations in the coastal ocean water column. The ISME journal Reji, L., Tolar, B. B., Smith, J. M., Chavez, F. P., Francis, C. A. 2019

    Abstract

    Ecological factors contributing to depth-related diversification of marine Thaumarchaeota populations remain largely unresolved. To investigate the role of potential microbial associations in shaping thaumarchaeal ecotype diversification, we examined co-occurrence relationships in a community composition dataset (16S rRNA V4-V5 region) collected as part of a 2-year time series in coastal Monterey Bay. Ecotype groups previously defined based on functional gene diversity-water column A (WCA), water column B (WCB) and Nitrosopumilus-like clusters-were recovered in the thaumarchaeal 16S rRNA gene phylogeny. Networks systematically reflected depth-related patterns in the abundances of ecotype populations, suggesting thaumarchaeal ecotypes as keystone members of the microbial community below the euphotic zone. Differential environmental controls on the ecotype populations were further evident in subnetwork modules showing preferential co-occurrence of OTUs belonging to the same ecotype cluster. Correlated abundances of Thaumarchaeota and heterotrophic bacteria (e.g., Bacteroidetes, Marinimicrobia and Gammaproteobacteria) indicated potential reciprocal interactions via dissolved organic matter transformations. Notably, the networks recovered ecotype-specific associations between thaumarchaeal and Nitrospina OTUs. Even at depths where WCB-like Thaumarchaeota dominated, Nitrospina OTUs were found to preferentially co-occur with WCA-like and Nitrosopumilus-like thaumarchaeal OTUs, highlighting the need to investigate the ecological implications of the composition of nitrifier assemblages in marine waters.

    View details for PubMedID 30610232

  • 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 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
  • Nutrient transport suggests an evolutionary basis for charged archaeal surface layer proteins. The ISME journal Li, P. N., Herrmann, J. n., Tolar, B. B., Poitevin, F. n., Ramdasi, R. n., Bargar, J. R., Stahl, D. A., Jensen, G. J., Francis, C. A., Wakatsuki, S. n., van den Bedem, H. n. 2018

    Abstract

    Surface layers (S-layers) are two-dimensional, proteinaceous, porous lattices that form the outermost cell envelope component of virtually all archaea and many bacteria. Despite exceptional sequence diversity, S-layer proteins (SLPs) share important characteristics such as their ability to form crystalline sheets punctuated with nano-scale pores, and their propensity for charged amino acids, leading to acidic or basic isoelectric points. However, the precise function of S-layers, or the role of charged SLPs and how they relate to cellular metabolism is unknown. Nano-scale lattices affect the diffusion behavior of low-concentration solutes, even if they are significantly smaller than the pore size. Here, we offer a rationale for charged S-layer proteins in the context of the structural evolution of S-layers. Using the ammonia-oxidizing archaea (AOA) as a model for S-layer geometry, and a 2D electrodiffusion reaction computational framework to simulate diffusion and consumption of the charged solute ammonium (NH4+), we find that the characteristic length scales of nanoporous S-layers elevate the concentration of NH4+ in the pseudo-periplasmic space. Our simulations suggest an evolutionary, mechanistic basis for S-layer charge and shed light on the unique ability of some AOA to oxidize ammonia in environments with nanomolar NH4+ availability, with broad implications for comparisons of ecologically distinct populations.

    View details for PubMedID 29899515

  • 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. n., Bargar, J. R., van den Bedem, H. n., Wakatsuki, S. n., 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 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