Honors & Awards

  • Graduate Research Fellowship, National Science Foundation (2014-)

Education & Certifications

  • BA, Washington University in St. Louis, Chemistry: Concentration in Biochemistry (2014)

All Publications

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


    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 DOI 10.1038/s41396-018-0191-0

    View details for PubMedID 29899515

  • Environmental Calcium Controls Alternate Physical States of the Caulobacter Surface Layer BIOPHYSICAL JOURNAL Herrmann, J., Jabbarpour, F., Bargar, P. G., Nomellini, J. F., Li, P., Lane, T. J., Weiss, T. M., Smit, J., Shapiro, L., Wakatsuki, S. 2017; 112 (9): 1841-1851


    Surface layers (S-layers) are paracrystalline, proteinaceous structures found in most archaea and many bacteria. Often the outermost cell envelope component, S-layers serve diverse functions including aiding pathogenicity and protecting against predators. We report that the S-layer of Caulobacter crescentus exhibits calcium-mediated structural plasticity, switching irreversibly between an amorphous aggregate state and the crystalline state. This finding invalidates the common assumption that S-layers serve only as static wall-like structures. In vitro, the Caulobacter S-layer protein, RsaA, enters the aggregate state at physiological temperatures and low divalent calcium ion concentrations. At higher concentrations, calcium ions stabilize monomeric RsaA, which can then transition to the two-dimensional crystalline state. Caulobacter requires micromolar concentrations of calcium for normal growth and development. Without an S-layer, Caulobacter is even more sensitive to changes in environmental calcium concentration. Therefore, this structurally dynamic S-layer responds to environmental conditions as an ion sensor and protects Caulobacter from calcium deficiency stress, a unique mechanism of bacterial adaptation. These findings provide a biochemical and physiological basis for RsaA's calcium-binding behavior, which extends far beyond calcium's commonly accepted role in aiding S-layer biogenesis or oligomerization and demonstrates a connection to cellular fitness.

    View details for DOI 10.1016/j.bpj.2017.04.003

    View details for Web of Science ID 000401301600013

    View details for PubMedID 28494955

  • 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


    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

  • Structural biology and regulation of the plant sulfation pathway CHEMICO-BIOLOGICAL INTERACTIONS Jez, J. M., Ravilious, G. E., Herrmann, J. 2016; 259: 31-38


    In plants, sulfur is an essential nutrient that must be converted into usable metabolic forms for the formation of sulfur-containing amino acids and peptides (primary route) and for the modification of diverse metabolites (secondary route). In plants, the fate of assimilated sulfate depends on the three enzymes - ATP sulfurylase, adenosine-5'-phosphate (APS) reductase, and APS kinase - that form a branchpoint in the pathway. ATP sulfurylase catalyzes the formation of the critical intermediate APS, which can either be used in the primary assimilatory route or be phosphorylated to 3'-phospho-APS (PAPS) for a variety of sulfation reactions. Recent biochemical and structural studies of the branchpoint enzymes in plant sulfur metabolism suggest that redox-regulation may control sulfur partitioning between primary and secondary routes. Disulfide-based redox switches differentially affect APS reductase and APS kinase. Oxidative conditions that promote disulfide formation increase the activity of APS reductase and decreases PAPS production by APS kinase. Here we review recent work on the ATP sulfurylase and APS kinase from plants that provide new insight on the regulation of PAPS formation, the structural evolution of these enzymes in different organisms, and redox-control of this key branchpoint in plant sulfur metabolism.

    View details for DOI 10.1016/j.cbi.2016.02.017

    View details for Web of Science ID 000388841600006

    View details for PubMedID 26926807

  • Recapitulating the Structural Evolution of Redox Regulation in Adenosine 5 '-Phosphosulfate Kinase from Cyanobacteria to Plants JOURNAL OF BIOLOGICAL CHEMISTRY Herrmann, J., Nathin, D., Lee, S. G., Sun, T., Jez, J. M. 2015; 290 (41): 24705-24714


    In plants, adenosine 5'-phosphosulfate (APS) kinase (APSK) is required for reproductive viability and the production of 3'-phosphoadenosine 5'-phosphosulfate (PAPS) as a sulfur donor in specialized metabolism. Previous studies of the APSK from Arabidopsis thaliana (AtAPSK) identified a regulatory disulfide bond formed between the N-terminal domain (NTD) and a cysteine on the core scaffold. This thiol switch is unique to mosses, gymnosperms, and angiosperms. To understand the structural evolution of redox control of APSK, we investigated the redox-insensitive APSK from the cyanobacterium Synechocystis sp. PCC 6803 (SynAPSK). Crystallographic analysis of SynAPSK in complex with either APS and a non-hydrolyzable ATP analog or APS and sulfate revealed the overall structure of the enzyme, which lacks the NTD found in homologs from mosses and plants. A series of engineered SynAPSK variants reconstructed the structural evolution of the plant APSK. Biochemical analyses of SynAPSK, SynAPSK H23C mutant, SynAPSK fused to the AtAPSK NTD, and the fusion protein with the H23C mutation showed that the addition of the NTD and cysteines recapitulated thiol-based regulation. These results reveal the molecular basis for structural changes leading to the evolution of redox control of APSK in the green lineage from cyanobacteria to plants.

    View details for DOI 10.1074/jbc.M115.679514

    View details for Web of Science ID 000362598300007

    View details for PubMedID 26294763

    View details for PubMedCentralID PMC4598983

  • Structure and mechanism of soybean ATP sulfurylase and the committed step in plant sulfur assimilation. journal of biological chemistry Herrmann, J., Ravilious, G. E., McKinney, S. E., Westfall, C. S., Lee, S. G., Baraniecka, P., Giovannetti, M., Kopriva, S., Krishnan, H. B., Jez, J. M. 2014; 289 (15): 10919-10929


    Enzymes of the sulfur assimilation pathway are potential targets for improving nutrient content and environmental stress responses in plants. The committed step in this pathway is catalyzed by ATP sulfurylase, which synthesizes adenosine 5'-phosphosulfate (APS) from sulfate and ATP. To better understand the molecular basis of this energetically unfavorable reaction, the x-ray crystal structure of ATP sulfurylase isoform 1 from soybean (Glycine max ATP sulfurylase) in complex with APS was determined. This structure revealed several highly conserved substrate-binding motifs in the active site and a distinct dimerization interface compared with other ATP sulfurylases but was similar to mammalian 3'-phosphoadenosine 5'-phosphosulfate synthetase. Steady-state kinetic analysis of 20 G. max ATP sulfurylase point mutants suggests a reaction mechanism in which nucleophilic attack by sulfate on the α-phosphate of ATP involves transition state stabilization by Arg-248, Asn-249, His-255, and Arg-349. The structure and kinetic analysis suggest that ATP sulfurylase overcomes the energetic barrier of APS synthesis by distorting nucleotide structure and identifies critical residues for catalysis. Mutations that alter sulfate assimilation in Arabidopsis were mapped to the structure, which provides a molecular basis for understanding their effects on the sulfur assimilation pathway.

    View details for DOI 10.1074/jbc.M113.540401

    View details for PubMedID 24584934

    View details for PubMedCentralID PMC4036203

  • Kinetic mechanism of the dimeric ATP sulfurylase from plants BIOSCIENCE REPORTS Ravilious, G. E., Herrmann, J., Lee, S. G., Westfall, C. S., Jez, J. M. 2013; 33: 585-591


    In plants, sulfur must be obtained from the environment and assimilated into usable forms for metabolism. ATP sulfurylase catalyses the thermodynamically unfavourable formation of a mixed phosphosulfate anhydride in APS (adenosine 5'-phosphosulfate) from ATP and sulfate as the first committed step of sulfur assimilation in plants. In contrast to the multi-functional, allosterically regulated ATP sulfurylases from bacteria, fungi and mammals, the plant enzyme functions as a mono-functional, non-allosteric homodimer. Owing to these differences, here we examine the kinetic mechanism of soybean ATP sulfurylase [GmATPS1 (Glycine max (soybean) ATP sulfurylase isoform 1)]. For the forward reaction (APS synthesis), initial velocity methods indicate a single-displacement mechanism. Dead-end inhibition studies with chlorate showed competitive inhibition versus sulfate and non-competitive inhibition versus APS. Initial velocity studies of the reverse reaction (ATP synthesis) demonstrate a sequential mechanism with global fitting analysis suggesting an ordered binding of substrates. ITC (isothermal titration calorimetry) showed tight binding of APS to GmATPS1. In contrast, binding of PPi (pyrophosphate) to GmATPS1 was not detected, although titration of the E•APS complex with PPi in the absence of magnesium displayed ternary complex formation. These results suggest a kinetic mechanism in which ATP and APS are the first substrates bound in the forward and reverse reactions, respectively.

    View details for DOI 10.1042/BSR20130073

    View details for Web of Science ID 000324032600005

    View details for PubMedID 23789618

    View details for PubMedCentralID PMC3728988

  • Structural Basis for Prereceptor Modulation of Plant Hormones by GH3 Proteins SCIENCE Westfall, C. S., Zubieta, C., Herrmann, J., Kapp, U., Nanao, M. H., Jez, J. M. 2012; 336 (6089): 1708-1711


    Acyl acid amido synthetases of the GH3 family act as critical prereceptor modulators of plant hormone action; however, the molecular basis for their hormone selectivity is unclear. Here, we report the crystal structures of benzoate-specific Arabidopsis thaliana AtGH3.12/PBS3 and jasmonic acid-specific AtGH3.11/JAR1. These structures, combined with biochemical analysis, define features for the conjugation of amino acids to diverse acyl acid substrates and highlight the importance of conformational changes in the carboxyl-terminal domain for catalysis. We also identify residues forming the acyl acid binding site across the GH3 family and residues critical for amino acid recognition. Our results demonstrate how a highly adaptable three-dimensional scaffold is used for the evolution of promiscuous activity across an enzyme family for modulation of plant signaling molecules.

    View details for DOI 10.1126/science.1221863

    View details for Web of Science ID 000305794500051

    View details for PubMedID 22628555

  • Modulating plant hormones by enzyme action: the GH3 family of acyl acid amido synthetases. Plant signaling & behavior Westfall, C. S., Herrmann, J., Chen, Q., Wang, S., Jez, J. M. 2010; 5 (12): 1607-1612


    Plants respond to developmental cues and environmental stresses by controlling both the level and activity of various hormones. One mechanism of modulating hormone action involves amino acid conjugation. In plants, the GH3 family of enzymes conjugates various amino acids to jasmonates, auxins, and benzoates. The effect of conjugation can lead to activation, inactivation, or degradation of these molecules. Although the acyl acid and amino acid specificities of a few GH3 enzymes have been examined qualitatively, further in-depth analysis of the structure and function of these proteins is needed to reveal the molecular basis for how GH3 proteins modulate plant hormone action.

    View details for PubMedID 21150301

    View details for PubMedCentralID PMC3115113