Since the beginning of the Auer Lab in 2004, we have expanded our research portfolio and focus significantly, adding to our initial focus on the
1. structural analysis of inner ear molecular machines a variety of other projects that fall into four main categories:
2. molecular mechanisms in cancer malignancy and metastasis with a focus on cell-cell adhesion patterns,
3. microbial communities (biofilms) including bioremediation, gliding motility, and the roles of vesicles in microbial communities,
4. bioenergy/biofuels including plant cell walls and lignocellulosic degradation, and
5. method development for correlative multiscale, multimodal imaging, including exploring several tag-based labeling approaches.
Our mission is to gain fundamental insight into biology, in part by visualizing molecular machines at molecular resolution, and to identify their protein composition through novel labeling approaches. While 2D electron microscopy and 3D electron tomography continue to be the major tools for the analysis of macromolecular machines in their native cellular environment, our tomographic studies are often complemented by biochemical, cell biological, biophysical and high-end optical and TEM and SEM imaging techniques, as well as computational data analysis including sophisticated visualization, segmentation and quantitative analysis. Although the task of studying supramolecular complexes in their native cellular environment is challenging, we feel rewarded by the discovery of the fascinating complexity of molecular machines. The models derived from our structural studies then often serve as a platform for further neurobiological, cell biological, pharmacological or microbiological testing. Where we do not possess the expertise in our own laboratory, we do collaborate with a variety of experts, both on the biological as well as the technical side.
The field of structural biology has an impressive record of 3D structures of proteins at atomic resolution, owing mostly to X-ray crystallography and NMR, with a small but significant contribution from cryo-electron microscopy. In recent years, biology at large has witnessed a paradigm shift: It is now widely recognized that fundamental cellular processes do not occur as the result of protein molecules colliding randomly within the cytoplasm or cell membrane, but that they are carried out by molecular machines which are composed of large numbers of individual proteins. As Richard Feynman put it in 1960: "It is very easy to answer many fundamental questions, you just need look at the thing!"
This is in essence our goal, to look at such molecular machines in sufficient detail in order to understand how they perform the function for which they have been optimized. For a cell at work, we can assume that a fair number of these complexes are transient, and variable in composition and conformation, and that they may not be abundant and stable enough to be isolated. Moreover, some of these complexes need to be in their exact cellular environment to function properly, e.g. they may need to be attached extracellularly to the surrounding matrix and intracellularly to the cytoskeleton. Although the exact composition and therefore the 3D structure of such complexes may vary within one cell at any given time, we would expect to detect an underlying building principle, which is necessary for their function. Such flexibility, scarcity and fragility exclude most structural techniques that explicitly or implicitly rely on averaging of identical components. Hence, for the study of such molecular machines, electron tomography is the most suitable technique to obtain 3D structural information, for it can visualize macromolecular assemblies in their natural cellular context, without the need for averaging. Tomographic imaging can retrieve this 3D information by capturing a series of images of the same object at different tilt angles. The different views of the projected volume are combined and projected back into a volume, a tomogram that represents the mass density.
Electron Tomography and Labeling
We employ electron tomography as a tool to investigate the architectural organization of macromolecular complexes, also known as molecular machines. Electron tomography is presumably the most generally applicable method that reaches to the resolution of individual protein molecules, while allowing the complex to reside in their native cellular context and is particularly well suited for the study of multi-protein complexes that are too rare or fragile to be purified. Examining electron tomograms reveals the complexity of cellular organization. We have helped to develop sophisticated tools for the visualization, segmentation and analysis of tomograms. Recently developed protocols avoid time-consuming manual segmentation and therefore speed up the analysis of the large density maps. However, in complex cellular environment, shape and size may not be sufficient to determine the molecular composition. Moreover, some components may be too small to be identified through a structural approach. Hence, we are also developing novel labeling approaches that are based on genetically encoded tags that can be recognized by universal labels, therefore avoiding the uncertainties often encountered by immuno-labeling methods. The identification of molecular components would tremendously aid in the interpretation of tomograms. This approach would allow the 3D localization of any candidate protein with high precision, provided the proteins can be genetically altered to include a tag.
Most cells are capable to mechanically sense their environment by ways that are largely unexplored. Mechanosensation is crucial for embryogenesis, for the organization of cells into tissues, as well as for the regulation of the function of a number of organs, e.g. the kidney, bones, muscle, etc. Mechanical clues are important in keeping cells alive and within their proper tissue context. Loss of contact of a cell with their neighboring cells or surrounding extracellular matrix often leads to apoptosis and is likely to be central to the mechanism of cancer pathogenesis. Mechanosensation lies at the core of the detection of sound, touch, pressure, gravity or magnetic fields. We have focused our attention on inner ear hair cells, which are central to our sense of hearing and balance.
1. Hearing Loss and Deafness: Inner Ear Hair Cells: Hair cells are -arguably- the most fascinating cell types present in vertebrates. Their malfunction lies at the heart of such devastating diseases as hearing loss deafness. One in 1000 children is born deaf, and about 10% of the population is affected by severe hearing loss. Hair cells are characterized by the hair bundle, which consists of stereocilia, highly specialized actin-based cell organelles. The mechanoelectrical transduction and adaptation machinery of hair cell stereocilia consists of extracellularly located fine filaments that connect two adjacent stereocilia and whose stretching results in the direct opening of mechanoelectrical transduction channels without the involvement of chemical messengers. The direct nature of mechanoelectrical transduction implies that adaptation to sustained stimuli is achieved by adjustment of the tension in the tip links via a movement of a non-conventional myosin along the actin filament bundle. We have determined the 3D architecture of the hair bundle extracellular linkers and measured the exact length of the basal, kinociliary and tip links and found that tip links are found as being either ~110 nm or ~170 nm long, raising questions about their identity. Furthermore we discovered an auxiliary link that has been overlooked so far and that may contribute to hair cell function. [Auer et al, 2008, JARO].
We are currently conducting several studies into the molecular organization of the hair bundle, including the actin bundle organization, the rootlets as well as the transduction and adaptation machinery. Read more about how we use electron tomography to unveil the secrets of these molecular machinesIn addition, we have conducted a thorough study on the 3D organization of the guinea pig outer hair cell lateral wall that hosts a prestin-based amplification machinery that consists of the plasma membrane, the underlying cortical lattice, consisting of actin patches and spectrin cross-links, as well as the underlying subsurface cisterna (SSC). We are collaborating with a variety of hearing researcher at Case Western Reserve University, University of Kentucky, Rice University, as well as Oregon Health and Science University on the structure and function of the hair bundle, the cuticular plate, as well as the stria vascularis.
2. Mammary Gland Biology and Breast Cancer: In collaboration with the laboratories of Mina Bissell (LBNL), Valerie Weaver (UCSF), Zena Werb (UCSF) and Andy Ewald (Johns Hopkins University–School of Medicine), we have studied the ultrastructure of human S1/T4 cell line in Matrigel as well as mouse breast organoids in Matrigel, respectively. We have focused our attention on the presence and distribution of cell-cell adhesion complexes and found a breakdown in apical-basolateral organization both for S1/T4 as well as for FGF2-stimulated mouse organoids, suggesting that changes in cell-cell adhesion play a role both for cancer progression as well as embryonal development.
3. Microbial Communities: We have studied the biofilm organization of Desulfovibrio vulgaris (DvH) and other sulfate reducers, Myxococcus xanthus, Acid Mine Drainage biofilms, lignocellulose-degrading termite hindgut community as well as a variety of other microbial communities.
We are intrigued by the patterns of extracellular metal depositons and the biofilm organization. We also found evidence of a prominent role of vesicles in such biofilms. Both the sulfate reducing bacteria such as DvH and the myxobacteria display fascinating properties, and one might argue that the exploration of microbial communities/biofilms is one of the main frontiers in understanding microbial life.
4. Biofuels - Plants and lignocellulosic degradation: We are part of both the DOE-funded Joint BioEnergy Institute (JBEI) as well as the BP-funded Energy Biosciences Institute (EBI), both of which aim to overcome the recalcitrance of lignocellulose through basic research of the plant cell wall characteristics as well as of the events of chemical/biochemical as well as microbial lignocellulose degradation. We use use a variety of biophysical techniques (including imaging) to characterize plant cell wall properties, as well as to visualize the effect of various treatment on the plant biomass. In the context of EBI our goal is to obtain a realistic model of plant cell walls through cryo-electron tomography.
5. Method Development for Correlative Multiscale Multimodal Imaging: In the course of electron tomographic analysis we learned that 3D structural analysis alone often does not lead to conclusive proof of the molecular composition. As a matter of fact, labeling of certain protein components nicely complements 3D architectural information about protein complexes. As part of the ongoing PCAP project (pcap.lbl.gov) we develop novel tag-based labeling approaches in anaerobic sulfate reducing bacteria, exploring SNAP-tag labeling followed by photoconversion. Beside the novel labeling approaches we are also utilizing recent developments in computational sciences, including immersive 3D visualization, segmentation and quantitative geometric analysis.
One key for correlative imaging in our view is that we study the exact same sample probe/specimen by multipe imaging modalities. This poses some challenges on sample preparation and data registration that we are currently addressing. Since we have recently been able to both retain fluorescence signals as well as Raman signals throughout dehydration and resin-embedding/polymerization, we consider correlative imaging not only doable but also highly desirable.
Multiscale, Multimodal Integrated BioImaging may well be the next frontier in understanding complex systems, and the localization of components through labeling or Raman Imaging, combined with ultrastructural 3D context, will ultimately provide spatial maps that will serve as the foundation for systems biology.
The Lab's Infrastructure
Our lab is housed in the Donner building at the north-east corner of the UC Berkeley campus (home of the "Free Speech Movement"), at the bottom of Cyclotron Road that leads to the main site of LBNL on the hill overlooking the Bay Area. Four groups in the Donner lab are dedicated to electron microscopy of macromolecules, covering a variety of data acquisition and 3D reconstruction schemes, and when combined offer an almost unique atmosphere of technical know-how. The cordial and informal atmosphere of the Berkeley lab and the strong sense of community make LBNL a great place to get outstanding science done.
Since we research demands an expertise in a broad range of science, spanning from developmental and cell and neurobiology to chemical and biochemical sample preparation, physical TEM imaging and computational data reconstruction, visualization and analysis, we collaborate with some of the best groups in their respective fields. For instance, we are collaborating with Kent McDonald (UC Berkeley) with respect to high pressure freezing and freeze-substitution as well as cryo-sectioning.
The microscope equipment we share is among the best in the world, featuring two Jeol 4000, a Jeol 3100 equipped with an in-column energy filter, a Tecnai T12, Technai F20, Philips CM200FEG as well as a FEI Titan microscope. Most microscopes are capable to record high-resolution data, both for tomography and single particle analysis. Moreover, we have access to two high pressure freezers (Baltec and Leica Empect 2), two LEICA AMW microwave processors, 5 ultramicrotomes, two of which equipped for cryo-sectioning, as well as equipment for SEM sample preparation and imaging.
The Lab's Philosophy
Our efforts are fueled by the excitement of scientific discovery, and we believe that studying important biological problems requires an atmosphere of true team spirit where everybody's contribution is important and welcome. We consider a true passion for science as the most important ingredient for doing good science, but also aim keep a healthy balance between work and life outside the lab.
- Remis JP, Wei D, Gorur A, Zemla M, Haraga J, Allen S, Witkowska HE, Costerton JW, Berleman JE, Auer M. Bacterial social networks: structure and composition of Myxococcus Xanthus outer membrane vesicle chains. Environ Microbiol. 2013 Jun 18. doi: 10.1111/1462-2920.12187.
- Chiniquy d, Varanasi P, Oh T, Harholt J, Katnelson J, Singh S, Auer M, Simmons B, Adams PD, Scheller HV, Ronald PC. Three Novel Genes Closely Related to the Arabidopsis IRX9, IRX9L and IRX14 Genes and their Roles in Xylan Biosynthesis. Front Plant Sci. 2013 Apr 10; 4:83. doi: 10.3389/fpls.2013.00083. Print 2013.
- Neng L, Zhang W, Hassan A, Zemla M, Kachelmeier A, Fridberger A, Auer M, Shi X. Isolation and culture of endothelial cells, pericytes and perivascular resident macrophage-like melanocytes from the young mouse ear. Nat Protoc. 2013 Mar 14;8(4):709-20. doi: 10.1038/nprot.2013.033. Epub 2013 Mar 14. PubMed PMID: 23493068.
- Varanasi P, Singh P, Auer M, Adams PD, Simmons BA, Singh S. Survey of renewable chemicals produced from lignocellulosic biomass during ionic liquid pretreatment. Biotechnol Biofuels. 2013 Jan 28;6(1):14. doi:10.1186/1754-6834-6-14. PubMed PMID: 23356589; PubMed Central PMCID: PMC3579681.
- Shin JB, Krey JF, Hassan A, Metlagel Z, Tauscher AN, Pagana JM, Sherman NE, Jeffery ED, Spinelli KJ, Zhao H, Wilmarth PA, Choi D, David LL, Auer M, Barr-Gillespie PG. Molecular architecture of the chick vestibular hair bundle. Nat Neurosci. 2013 Mar;16(3):365-74. doi: 10.1038/nn.3312. Epub 2013 Jan 20. PubMed PMID: 23334578; PubMed Central PMCID: PMC3581746.
- Berleman J, Auer M. The role of bacterial outer membrane vesicles for intra- and interspecies delivery. Environ Microbiol. 2013 Feb;15(2):347-54. doi: 10.1111/1462-2920.12048. Epub 2012 Dec 11. PubMed PMID: 23227894.
- Petersen PD, Lau J, Ebert B, Yang F, Verhertbruggen Y, Kim JS, Varanasi P, Suttangkakul A, Auer M, Loqué D, Scheller HV. Engineering of plants with improved properties as biofuels feedstocks by vessel-specific complementation of xylan biosynthesis mutants. Biotechnol Biofuels. 2012 Nov 26;5(1):84. doi: 10.1186/1754-6834-5-84. PubMed PMID: 23181474; PubMed Central PMCID: PMC3537538.
- Chen X, Vega-Sánchez ME, Verhertbruggen Y, Chiniquy D, Canlas PE, Fagerström A, Prak L, Christensen U, Oikawa A, Chern M, Zuo S, Lin F, Auer M, Willats WG, Bartley L, Harholt J, Scheller HV, Ronald PC. Inactivation of OsIRX10 Leads to Decreased Xylan Content in Rice Culm Cell Walls and Improved Biomass Saccharification. Mol Plant. 2013 Mar;6(2):570-3. doi: 10.1093/mp/sss135. Epub 2012 Nov 23. PubMed PMID: 23180670.
- Yang F, Mitra P, Zhang L, Prak L, Verhertbruggen Y, Kim JS, Sun L, Zheng K, Tang K, Auer M, Scheller HV, Loqué D. Engineering secondary cell wall deposition in plants. Plant Biotechnol J. 2013 Apr;11(3):325-35. doi: 10.1111/pbi.12016. Epub 2012 Nov 12. PubMed PMID: 23140549.
- Varanasi P, Singh P, Arora R, Adams PD, Auer M, Simmons BA, Singh S. Understanding changes in lignin of Panicum virgatum and Eucalyptus globulus as a function of ionic liquid pretreatment. Bioresour Technol. 2012 Dec;126:156-61. doi: 10.1016/j.biortech.2012.08.070. Epub 2012 Aug 31. PubMed PMID: 23073103.
- Zhang W, Dai M, Fridberger A, Hassan A, Degagne J, Neng L, Zhang F, He W, Ren T, Trune D, Auer M, Shi X. Perivascular-resident macrophage-like melanocytes in the inner ear are essential for the integrity of the intrastrial fluid-blood barrier. Proc Natl Acad Sci U S A. 2012 Jun 26;109(26):10388-93. doi: 10.1073/pnas.1205210109. Epub 2012 Jun 11. PubMed PMID: 22689949; PubMed Central PMCID: PMC3387119.
- Baelum J, Borglin S, Chakraborty R, Fortney JL, Lamendella R, Mason OU, Auer M, Zemla M, Bill M, Conrad ME, Malfatti SA, Tringe SG, Holman HY, Hazen TC, Jansson JK. Deep-sea bacteria enriched by oil and dispersant from the Deepwater Horizon spill. Environ Microbiol. 2012 Sep;14(9):2405-16. doi: 10.1111/j.1462-2920.2012.02780.x. Epub 2012 May 23. PubMed PMID: 22616650.
- Parsons HT, Christiansen K, Knierim B, Carroll A, Ito J, Batth TS, Smith-Moritz AM, Morrison S, McInerney P, Hadi MZ, Auer M, Mukhopadhyay A, Petzold CJ, Scheller HV, Loqué D, Heazlewood JL. Isolation and proteomic characterization of the Arabidopsis Golgi defines functional and novel components involved in plant cell wall biosynthesis. Plant Physiol. 2012 May;159(1):12-26. doi: 10.1104/pp.111.193151. Epub 2012 Mar 19. PubMed PMID: 22430844; PubMed Central PMCID: PMC3375956.
- Ewald AJ, Huebner RJ, Palsdottir H, Lee JK, Perez MJ, Jorgens DM, Tauscher AN, Cheung KJ, Werb Z, Auer M. Mammary collective cell migration involves transient loss of epithelial features and individual cell migration within the epithelium. J Cell Sci. 2012 Jun 1;125(Pt 11):2638-54. doi: 10.1242/jcs.096875. Epub 2012 Feb 17. PubMed PMID: 22344263; PubMed Central PMCID: PMC3403234.
- Carlson HK, Iavarone AT, Gorur A, Yeo BS, Tran R, Melnyk RA, Mathies RA, Auer M, Coates JD. Surface multiheme c-type cytochromes from Thermincola potens and implications for respiratory metal reduction by Gram-positive bacteria. Proc Natl Acad Sci U S A. 2012 Jan 31;109(5):1702-7. doi: 10.1073/pnas.1112905109. Epub 2012 Jan 17. PubMed PMID: 22307634; PubMed Central PMCID: PMC3277152.
- Chhabra SR, Butland G, Elias DA, Chandonia JM, Fok OY, Juba TR, Gorur A, Allen S, Leung CM, Keller KL, Reveco S, Zane GM, Semkiw E, Prathapam R, Gold B, Singer M, Ouellet M, Szakal ED, Jorgens D, Price MN, Witkowska HE, Beller HR, Arkin AP, Hazen TC, Biggin MD, Auer M, Wall JD, Keasling JD. Generalized schemes for high-throughput manipulation of the Desulfovibrio vulgaris genome. Appl Environ Microbiol. 2011 Nov;77(21):7595-604. doi: 10.1128/AEM.05495-11. Epub 2011 Sep 9. PubMed PMID: 21908633; PubMed Central PMCID: PMC3209177.
- Wrighton KC, Thrash JC, Melnyk RA, Bigi JP, Byrne-Bailey KG, Remis JP, Schichnes D, Auer M, Chang CJ, Coates JD. Evidence for direct electron transfer by a gram-positive bacterium isolated from a microbial fuel cell. Appl Environ Microbiol. 2011 Nov;77(21):7633-9. doi: 10.1128/AEM.05365-11. Epub 2011 Sep 9. PubMed PMID: 21908627; PubMed Central PMCID: PMC3209153.
- Yin L, Verhertbruggen Y, Oikawa A, Manisseri C, Knierim B, Prak L, Jensen JK, Knox JP, Auer M, Willats WG, Scheller HV. The cooperative activities of CSLD2, CSLD3, and CSLD5 are required for normal Arabidopsis development. Mol Plant. 2011 Nov;4(6):1024-37. doi: 10.1093/mp/ssr026. Epub 2011 Apr 6. PubMed PMID: 21471331.
- Miroshnikova YA, Jorgens DM, Spirio L, Auer M, Sarang-Sieminski AL, Weaver VM. Engineering strategies to recapitulate epithelial morphogenesis within synthetic three-dimensional extracellular matrix with tunable mechanical properties. Phys Biol. 2011 Apr;8(2):026013. doi: 10.1088/1478-3975/8/2/026013. Epub 2011 Mar 25. PubMed PMID: 21441648; PubMed Central PMCID: PMC3401181.
- Vega-Sánchez ME, Verhertbruggen Y, Christensen U, Chen X, Sharma V, Varanasi P, Jobling SA, Talbot M, White RG, Joo M, Singh S, Auer M, Scheller HV, Ronald PC. Loss of Cellulose synthase-like F6 function affects mixed-linkage glucan deposition, cell wall mechanical properties, and defense responses in vegetative tissues of rice. Plant Physiol. 2012 May;159(1):56-69. doi: 10.1104/pp.112.195495. Epub 2012 Mar 2. PubMed PMID: 22388489; PubMed Central PMCID: PMC3375985.
- Bharadwaj R, Wong A, Knierim B, Singh S, Holmes BM, Auer M, Simmons BA, Adams PD, Singh AK. High-throughput enzymatic hydrolysis of lignocellulosic biomass via in-situ regeneration. Bioresour Technol. 2011 Jan;102(2):1329-37. doi: 10.1016/j.biortech.2010.08.108. Epub 2010 Sep 29. PubMed PMID: 20884206.
- Hazen TC, Dubinsky EA, DeSantis TZ, Andersen GL, Piceno YM, Singh N, Jansson JK, Probst A, Borglin SE, Fortney JL, Stringfellow WT, Bill M, Conrad ME, Tom LM, Chavarria KL, Alusi TR, Lamendella R, Joyner DC, Spier C, Baelum J, Auer M, Zemla ML, Chakraborty R, Sonnenthal EL, D'haeseleer P, Holman HY, Osman S, Lu Z, Van Nostrand JD, Deng Y, Zhou J, Mason OU. Deep-sea oil plume enriches indigenous oil-degrading bacteria. Science. 2010 Oct 8;330(6001):204-8. Doi: 10.1126/science.1195979. Epub 2010 Aug 24. PubMed PMID: 20736401.
- Remis JP, Costerton JW, Auer M. Biofilms: structures that may facilitate cell-cell interactions. ISME J. 2010 Sep;4(9):1085-7. doi: 10.1038/ismej.2010.105. Epub 2010 Jul 15. PubMed PMID: 20631806.
- Kent MS, Cheng G, Murton JK, Carles EL, Dibble DC, Zendejas F, Rodriquez MA, Tran H, Holmes B, Simmons BA, Knierim B, Auer M, Banuelos JL, Urquidi J, Hjelm RP. Study of enzymatic digestion of cellulose by small angle neutron scattering. Biomacromolecules. 2010 Feb 8;11(2):357-68. doi: 10.1021/bm9008952. PubMed PMID: 20041636.
- Li C, Knierim B, Manisseri C, Arora R, Scheller HV, Auer M, Vogel KP, Simmons BA, Singh S. Comparison of dilute acid and ionic liquid pretreatment of switchgrass: Biomass recalcitrance, delignification and enzymatic saccharification. Bioresour Technol. 2010 Jul;101(13):4900-6. doi: 10.1016/j.biortech.2009.10.066. Epub 2009 Nov 30. PubMed PMID: 19945861.
- Sarkar P, Bosneaga E, Auer M. Plant cell walls throughout evolution: towards a molecular understanding of their design principles. J Exp Bot. 2009;60(13):3615-35. doi: 10.1093/jxb/erp245. Epub 2009 Aug 17. Review. PubMed PMID: 19687127.
- DeBolt S, Scheible WR, Schrick K, Auer M, Beisson F, Bischoff V, Bouvier-Navé P, Carroll A, Hematy K, Li Y, Milne J, Nair M, Schaller H, Zemla M, Somerville C. Mutations in UDP-Glucose:sterol glucosyltransferase in Arabidopsis cause transparent testa phenotype and suberization defect in seeds. Plant Physiol. 2009 Sep;151(1):78-87. doi: 10.1104/pp.109.140582. Epub 2009 Jul 29. PubMed PMID: 19641030; PubMed Central PMCID: PMC2735980.
- Schmidt M, Schwartzberg AM, Perera PN, Weber-Bargioni A, Carroll A, Sarkar P, Bosneaga E, Urban JJ, Song J, Balakshin MY, Capanema EA, Auer M, Adams PD, Chiang VL, Schuck PJ. Label-free in situ imaging of lignification in the cell wall of low lignin transgenic Populus trichocarpa. Planta. 2009 Aug;230(3):589-97. doi: 10.1007/s00425-009-0963-x. Epub 2009 Jun 13. PubMed PMID: 19526248; PubMed Central PMCID: PMC2715566.
- Palsdottir H, Remis JP, Schaudinn C, O'Toole E, Lux R, Shi W, McDonald KL, Costerton JW, Auer M. Three-dimensional macromolecular organization of cryofixed Myxococcus xanthus biofilms as revealed by electron microscopic tomography. J Bacteriol. 2009 Apr;191(7):2077-82. doi: 10.1128/JB.01333-08. Epub 2009 Jan 23. PubMed PMID: 19168614; PubMed Central PMCID: PMC2655519.
- Shawkey MD, Saranathan V, Pálsdóttir H, Crum J, Ellisman MH, Auer M, Prum RO. Electron tomography, three-dimensional Fourier analysis and colour prediction of a three-dimensional amorphous biophotonic nanostructure. J R Soc Interface. 2009 Apr 6;6 Suppl 2:S213-20. doi: 10.1098/rsif.2008.0374.focus. Epub 2009 Jan 20. PubMed PMID: 19158016; PubMed Central PMCID: PMC2706473.
- Wilmes P, Remis JP, Hwang M, Auer M, Thelen MP, Banfield JF. Natural acidophilic biofilm communities reflect distinct organismal and functional organization. ISME J. 2009 Feb;3(2):266-70. doi: 10.1038/ismej.2008.90. Epub 2008 Oct 9. PubMed PMID: 18843299.
- Triffo WJ, Palsdottir H, McDonald KL, Lee JK, Inman JL, Bissell MJ, Raphael RM, Auer M. Controlled microaspiration for high-pressure freezing: a new method for ultrastructural preservation of fragile and sparse tissues for TEM and electron tomography. J Microsc. 2008 May;230(Pt 2):278-87. doi: 10.1111/j.1365-2818.2008.01986.x. PubMed PMID: 18445158; PubMed Central PMCID: PMC2734140.
- Auer M, Koster AJ, Ziese U, Bajaj C, Volkmann N, Wang da N, Hudspeth AJ. Three-dimensional architecture of hair-bundle linkages revealed by electron-microscopic tomography. J Assoc Res Otolaryngol. 2008 Jun;9(2):215-24. doi: 10.1007/s10162-008-0114-2. Epub 2008 Apr 18. PubMed PMID: 18421501; PubMed Central PMCID: PMC2504599.
- Downing KH, Sui H, Auer M. Electron tomography: a 3D view of the subcellular world. Anal Chem. 2007 Nov 1;79(21):7949-57. Review. PubMed PMID: 18044021.
- Persson S, Paredez A, Carroll A, Palsdottir H, Doblin M, Poindexter P, Khitrov N, Auer M, Somerville CR. Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc Natl Acad Sci U S A. 2007 Sep 25;104(39):15566-71. Epub 2007 Sep 18. PubMed PMID: 17878302; PubMed Central PMCID: PMC2000526.
- Schaber JA, Triffo WJ, Suh SJ, Oliver JW, Hastert MC, Griswold JA, Auer M, Hamood AN, Rumbaugh KP. Pseudomonas aeruginosa forms biofilms in acute infection independent of cell-to-cell signaling. Infect Immun. 2007 Aug;75(8):3715-21. Epub 2007 Jun 11. PubMed PMID: 17562773; PubMed Central PMCID: PMC1952004.
- McDonald KL, Auer M. High-pressure freezing, cellular tomography, and structural cell biology. Biotechniques. 2006 Aug;41(2):137, 139, 141 passim. Review. PubMed PMID: 16925014.
- Bajaj C, Yu Z, Auer M. Volumetric feature extraction and visualization of tomographic molecular imaging. J Struct Biol. 2003 Oct-Nov;144(1-2):132-43. PubMed PMID: 14643216.
- Lemieux MJ, Song J, Kim MJ, Huang Y, Villa A, Auer M, Li XD, Wang DN. Three-dimensional crystallization of the Escherichia coli glycerol-3-phosphate transporter: a member of the major facilitator superfamily. Protein Sci. 2003 Dec;12(12):2748-56. PubMed PMID: 14627735; PubMed Central PMCID: PMC2366983.
- Huang Y, Lemieux MJ, Song J, Auer M, Wang DN. Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science. 2003 Aug 1;301(5633):616-20. PubMed PMID: 12893936.
- Auer M, Kim MJ, Lemieux MJ, Villa A, Song J, Li XD, Wang DN. High-yield expression and functional analysis of Escherichia coli glycerol-3-phosphate transporter. Biochemistry. 2001 Jun 5;40(22):6628-35. PubMed PMID: 11380257.
- Li XD, Villa A, Gownley C, Kim MJ, Song J, Auer M, Wang DN. Monomeric state and ligand binding of recombinant GABA transporter from Escherichia coli. FEBS Lett. 2001 Apr 13;494(3):165-9. PubMed PMID: 11311234.
- Auer M. Three-dimensional electron cryo-microscopy as a powerful structural tool in molecular medicine. J Mol Med (Berl). 2000;78(4):191-202. Review. PubMed PMID: 10933581.
- Lancaster CR, Kröger A, Auer M, Michel H. Structure of fumarate reductase from Wolinella succinogenes at 2.2 A resolution. Nature. 1999 Nov 25;402(6760):377-85. PubMed PMID: 10586875.
- Stokes DL, Auer M, Zhang P, Kühlbrandt W. Comparison of H+-ATPase and Ca2+-ATPase suggests that a large conformational change initiates P-type ion pump reaction cycles. Curr Biol. 1999 Jul 1;9(13):672-9. PubMed PMID: 10395538.
- Auer M, Scarborough GA, Kühlbrandt W. Surface crystallisation of the plasma membrane H+-ATPase on a carbon support film for electron crystallography. J Mol Biol. 1999 Apr 16;287(5):961-8. PubMed PMID: 10222203.
- Kühlbrandt W, Auer M, Scarborough GA. Structure of the P-type ATPases. Curr Opin Struct Biol. 1998 Aug;8(4):510-6. Review. PubMed PMID: 9729744.
- Auer M, Scarborough GA, Kühlbrandt W. Three-dimensional map of the plasma membrane H+-ATPase in the open conformation. Nature. 1998 Apr 23;392(6678):840-3. PubMed PMID: 9572146.
- Cyrklaff M, Auer M, Kühlbrandt W, Scarborough GA. 2-D structure of the Neurospora crassa plasma membrane ATPase as determined by electron cryomicroscopy. EMBO J. 1995 May 1;14(9):1854-7. PubMed PMID: 7743992; PubMed Central PMCID: PMC398284.
In the News
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Videos from the Lab
A Bacterial Social Network:
AlumniYajima, Yuka (2012-2013), AIST, Japan
Bradley, Chelsea (Summer 2013)
Correa, Joaquin (2012-2013), CRD, LBNL
Jorgens, Danielle (2005 – 2013), postdoc OHSU
Tauscher, Andrew (2008-2013), now in San Francisco
Tsai, Wenting (2010 – 2013), Ph.D. student UCLA
Apte, Salil (2012) IIT, Energo Group New Delhi, India
Biddle, Amy (2007), Ph.D candidate UMass
Bosneaga, Elena (2007-2011), India
Chang, Timothy (2008 – 2009), B.S UCLA
Chatterjee, Gourab (2008, 2009), Ph.D. candidate UWashington, MO
Das, Jyotirmoy (2012) IIT, Robert Bosch R&D - Bangalore, India
Fagorala, Afolami (2006, 2008)
Faraji, Farshid (2006-2008)
Hildur Palsdottir (2004- 2008), Long Island, NY
Knierim, Bernhard (2007-2010), Germany
Kumar, Shailabh (2008, 2009), Ph.D. candidate UMinnesota, MN
Lee, Jessie K (2005-2010), UCB School of Ophtalmology
Lin, Monica (2009-2012), B.S UC Berkeley
Maji, Dolonchampa (2009), Ph.D. candidate Washington U. School of Medicine
Manansala, Miguel (2006), Ph.D. candidate UC Merced
Mondal, Poulami (2008)
Myhanh Duong (2007)
Natesan, Alamelu (2010-2011)
Padilla, Cesar (2006), Medical School
Perez, Melissa (2006-2011), Medical School
Peril, Özgül (2007-2010), University of Istanbul, Turkey
Prak, Lina (2007-2010), East Coast, US
Remis, Jonathan (2005-2012), Northwestern University
Shah, Mansi (2010-2011)
Triffo, Jeff (2005-2011), Residency Program, Wake Forest University
Warnke, Dwight F. (2005), High School teacher
Webb, Rick(2008-2009), University of Queenland, Australia
Zhang, Robin (2006, 2007)