Peer-reviewed publications and book chapters

member of Hatzenpichler lab       shared first authorship       * corresponding author

25Marlow JJ, Spietz RL, Kim K, Ellisman M, Girguis P, Hatzenpichler R*. Spatially-resolved correlative microscopy and microbial identification reveals dynamic depth- and mineral-dependent anabolic activity in salt marsh sediment. In revision   Pre-print

​BONCAT, resin embedding, and correlative fluorescence and electron microscopy are combined to reveal the spatial patterning of anabolically active cells around specific minerals in heterogenous salt marsh sediment. 

24. Reichart NJ, Bowers R, Woyke T, Hatzenpichler R*​. High potential for biomass-degrading enzymes revealed by hot spring metagenomics. Front Microbiol, 12: 668238 (2021)   PDF

Deals with the taxonomic diversity and carbohydrate active enzyme coding potential in 71 metagenomes from 58 hot springs.​

23. Hu D, Cui Y, Markillie LM, Chrisler WB, Wang Q, Hatzenpichler R, Orr G. Counting mRNA copies in intact bacterial cells by fluctuation localization imaging-based fluorescence in situ hybridization (fliFISH). Book chapter for Fluorescence In Situ Hybridization (FISH) for Microbial Cells: Methods and Concepts, Methods in Molecular Biology, Azevedo N.F & Almeida C (eds.), Vol. 2246, 237-247, Springer Nature (2021)   PDF

fliFISH uses on/off cycles of photo-switching dyes to set a predetermined threshold for distinguishing true signal from background noise.

2​​​​2. Nayfach S, Roux S, Seshadri R, Udwary D, Varghese N, Schulz F, Wu D, Paez-Espino D, Chen IM, Huntemann M, Palaniappan K, Ladau J, Mukherjee S, Reddy TBK, Nielsen T, Kirton E, Faria JP, Edirisinghe JN, Henry CS, Jungbluth SP, Chivian D, Dehal P, Wood-Charlson EM, Arkin AP, Tringe SG, Visel A, IMG/M Data Consortium, Woyke T, Mouncey NJ, Ivanova NN, Kyrpides NC, Eloe-Fadrosh EA. A genomic catalog of Earth's microbiomes. Nat Biotech, DOI:10.1038/s41587-020-0718-6 (2020)   PDF   JGI press release

A catalog of 52,515 metagenome-assembled genomes (MAGs) representing 12,556 novel candidate species-level operational taxonomic units spanning 135 phyla. Our lab contributed 45 MAGs from a salt marsh metagenome but we were not involved in any data analyses.

21. Reichart NJ, Jay ZJ, Krukenberg V, Parker AE, Spietz RL, Hatzenpichler R*Activity-based cell sorting reveals responses of uncultured archaea and bacteria to substrate amendment. The ISME J, 14: 2851–2861 (2020)   PDF   Behind the paper post
We use BONCAT-FACS to detect changes in the translational activity of a hot spring microbial community that was incubated in the presence of various potential growth substrates and different oxygen levels.

20. Murray AE, Freudenstein J, Gribaldo S, Hatzenpichler R, Hugenholtz P, Hedlund BP, Reysenbach A-L, et al. Roadmap for naming uncultivated archaea and bacteria. Nat Microbiol, 5: 987–994 (2020)   PDF   Press release

Consensus statement ​​proposing two potential paths forward towards solving the problem of naming uncultured archaea and bacteria.

19. ​Steward KF, Eilers B, Tripet B, Fuchs A, Dorle M, Rawle R, Soriano B, Balasubramanian N, Copié V, Bothner B*, Hatzenpichler R*Metabolic Implications of Using BioOrthogonal Non-Canonical Amino Acid Tagging (BONCAT) for Tracking Protein Synthesis​. Front Microbiol, 11:197 (2020)   PDF

Growing E. coli with AHA or HPG alters ~15 % of global mass features (LC-MS). 7 % change if cells are grown on methionine.

18. Hatzenpichler R*, Krukenberg V, Spietz RL, Jay ZJNext-generation physiology approaches to study microbiome function at the single cell level. Nat Rev Microbiol, 18: 241-256 (2020)  PDF

>Review article

​Introduces the concept of "next-generation physiology". These approaches are defined as any combination of techniques that allow for non-destructive phenotypic characterization of single cells, enabling phenotype-based separation of the cell for downstream analyses. 

17. Lawson CE, Harcombe WR, Hatzenpichler R, Lindemann SR, Löffler F, O’Malley MA, García-Martin H, Pfleger BF, Raskin L, Venturelli OS, Weissbrodt DG, Noguera DR, McMahon KD. Unmasking common principles and practices for microbiome engineering. Nat Rev Microbiol, 17: 725–741 (2019)   PDF

>Perspective article

​​Discusses key elements of an iterative design-build-test-learn (DBTL) cycle for microbiome engineering applicable to all systems. 

16. ​McKay LJ, Hatzenpichler R, Inskeep WP, and Fields MW. Occurrence and expression of novel methyl-coenzyme M reductase gene (mcrA) variants in hot spring sediments. Nat Sci Rep, 7: 7252 (2017)   PDF

McrA genes, encoding the key enzyme for methanogenesis/methane oxidation, are expressed in Yellowstone National Park hot springs. 

15. Marlow JJ and Hatzenpichler R. Assessing metabolic activity at methane seeps: a testing ground for slow-growing environmental systems. Book chapter in Life at Vents and Seeps. p223-259 (2017)   PDF

A review of approaches allowing to shed light on microbial in situ activities, with a strong emphasis on deep-sea methane seeps.  

Hatzenpichler publications prior to starting faculty position at MSU

14. Tavormina PL, Hatzenpicher R, McGlynn SE, Chadwick G, Dawson K, Connon S, and Orphan VJ. Methyloprofundus. Book chapter in Bergey’s Manual of Systematics of Archaea and Bacteria. John Wiley & Sons, Inc. doi: 10.1002/9781118960608.gbm01414 (2016)   PDF
Description of genus Methyloprofundus and its type species M. sedimenti isolated from deep-sea sediment.

13. Miranda PJ, McLain N, Hatzenpichler R, Orphan VJ, Dillon JG. Characterization of chemosynthetic microbial mats associated with intertidal hydrothermal sulfur vents in White Point, San Pedro, CA. Front Microbiol, 7: 1163 (2016)   PDF

Diversity, micron-scale spatial associations, and metabolic activity of sulfate-reducers and sulfur-oxidizers in a microbial mat community.

12. Hatzenpichler R*, Connon SA, Goudeau D, Malmstrom RR, Woyke T, and Orphan VJ*. Visualizing in situ translational activity for identifying and sorting slow-growing archaeal-bacterial consortia. Proc Natl Acad Sci U.S.A., 113: E4069-E4078 (2016)   PDF

>Covered by a 'News & Views' article in Nat Microbiol     >Press release by the DOE Joint Genome Institute

Development of activity-based cell sorting via BONCAT-FACS. Discovery of Verrucomicrobial-Archaeal consortia in methane seep sediments via BONCAT-FACS. Demonstrates, for the first time, that all major sub-clades of ANME are active under controlled conditions.

11. Hatzenpichler R* and Orphan VJ. Detection of protein-synthesizing microorganisms in the environment via bioorthogonal non-canonical amino acid tagging (BONCAT). Book chapter for Hydrocarbon and Lipid Microbiology Protocols, Vol. 7: Single-cell and single-molecule methods. Springer Protocols Handbooks, DOI 10.1007/8623_2015_61 (2015)   PDF

Provides a description of how to design and perform BONCAT experiments using the two bioorthogonal amino acids AHA and HPG.

10. Tavormina PL, Hatzenpichler R, McGlynn S, Chadwick G, Dawson K, Connon S, and Orphan VJ. Methyloprofundus sedimenti gen. nov., sp. nov., an obligate methanotroph from ocean sediment belonging to the Deep Sea 1 clade of marine methanotrophs. Int J Syst Evo Microbiol, 65: 251–259 (2015)   PDF

​Reports the isolation and growth characteristics of the gammaproteobacterial methane-oxidizer Methylococcaceae strain WF1.

9. Ma L, Kim J, Hatzenpichler R, Karymov MA, Hubert N, Hanan IM, Chang EB, and Ismagilov RF. Gene-targeted microfluidic cultivation validated by isolation of a gut bacterium listed in Human Microbiome Project’s Most Wanted taxa. Proc Natl Acad Sci USA, 111: 9768–9773 (2014)   PDF

Describes a microfluidics-based workflow for genetically targeted isolation and cultivation of microbes from clinical samples.

8. Hatzenpichler R*, Scheller S, Tavormina PL, Babin B, Tirrell D, and Orphan VJ* In situ visualization of newly synthesized proteins in environmental microbes using amino acid tagging and click chemistry. Environ Microbiol, 16: 2568–2590(2014)     PDF

>Cover article   >Covered by a 'Research Highlight' in Environ Microbiol

Describes the first application of bioorthogonal labeling and click chemistry for fluorescent tracking of protein synthesis in individual, FISH-identified cells within environmental samples.

7. Lebedeva EV, Hatzenpichler R, Pelletier E, Schuster N, Hauzmayer S, Bulaev A, Grigorjeva NV, Galushko A, Schmid M, Palatinsky M, Le Paslier D, Daims H, and Wagner M. Enrichment and genome sequence of the group I.1a ammonia-oxidizing archaeon “Ca. Nitrosotenuis uzonensis” representing a clade globally distributed in thermal habitats. PLoS One, 8: e80835 (2013)   PDF

Reports on the enrichment and draft genome of a novel, moderately thermophilic group I.1a ammonia-oxidizing archaeon. 

6. Hatzenpichler R*. Diversity, physiology and niche differentiation of ammonia-oxidizing archaea. Appl Environ Microbiol, 78: 7501-7510 (2012)   PDF

>Review article   

A review of our current knowledge of the diversity and physiology of ammonia-oxidizing archaea, the factors controlling their ecology, and their role in the biogeochemical cycling of carbon and nitrogen.

5. Spang A, Poehlein A, Offre P, Zumbrägel S, Haider S, Rychlik N, Nowka B, Schmeisser C, Lebedeva E, Rattei T, Bӧhm C, Schmid M, Galushko A, Hatzenpichler R, Weinmaier T, Daniel R, Schleper C, Spieck E, Streit W, and Wagner M. The genome of the ammonia-oxidizing Candidatus Nitrososphaera gargensis: Insights into metabolic versatility and environmental adaptations. Environ Microbiol, 14: 3122–3145 (2012)   PDF

Reports the complete genome sequence of group I.1b AOA Ca. Nitrososphaera gargensis from a geothermal spring..

4. Mußmann M, Brito I, Pitcher A, Damsté JS, Hatzenpichler R, Richter A, Nielsen JL, Nielsen P H, Müller A, Daims H, Wagner M, and Head IM. Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. Proc Natl Acad Sci U.S.A., 108: 16771-16776 (2011)   PDF

Demonstrates that some amoA gene-carrying and expressing group I.1b thaumarchaeotes are not obligate chemolithoautotrophs.

3. Shapiro OH, Hatzenpichler R*, Buckley DH, Zinder SH, and Orphan VJ. Multicellular photo-magnetotactic bacteria. Environ Microbiol Rep, 3: 233–238 (2011)   PDF

>Chief Editor’s Choice Article 2011   

Reports a newly discovered phototactic behavior of multicellular magnetotactic bacteria from salt marsh sediment.

2. Spang A, Hatzenpichler R, Brochier-Armanet C, Rattei T, Tischler P, Spieck E, Streit W, Stahl DA, Wagner M, and Schleper C. Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends Microbiol 18:331-40 (2010)    PDF

>Cover article   >Most cited TiM-paper of interval 2010-2015 

Confirms the assignment of three novel archaea to the proposed phylum Thaumarchaeota and reveals a lineage-specific set of core informational processing genes.

1. Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H, and Wagner M. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc Natl Acad Sci U.S.A., 105: 2134-2139 (2008)   PDF

Reports enrichment and ecophysiological characterization of the ammonia-oxidizing archaeon Ca. Nitrososphaera gargensis, and provides first evidence that ammonia concentration is a niche-differentiating factor between archaeal and bacterial ammonia oxidizers.