Peer-reviewed publications and book chapters

member of Hatzenpichler lab       shared authorship position       * corresponding author

Accepted. Schaible GA, Jay JJ, Cliff J, Schulz F, Gauvin C, Goudeau D, Ruff E, Malmstrom RR, Edgcomb V, Hatzenpichler R*. Multicellular magnetotactic bacterial consortia are metabolically differentiated and not clonal.  PLoS Biology, accepted, 10.1371/journal.pbio.3002638   PDF preprint

We study the only known example of bacteria without a unicellular stage in their life cycle. Using a combination of single consortia metagenomics, species-resolved genome annotation, stable isotope probing, Nano-scale secondary ion mass spectrometry, fluorescence in situ hybridization, and bioorthogonal non-canonical amino acid tagging we show that cells within individual MMB consortia are not clonal and that they express dramatically different levels of anabolic activity.

Accepted. Kohtz AJ, Petrosian N, Krukenberg V,Jay ZJ, Pilhofer M, Hatzenpichler R*.Cultivation and visualization of a methanogen of the phylum Thermoproteota. Nature, accepted (DOI: 10.1038/s41586-024-07631-6)   Preprint PDF

Cultivation, physiology, and CryoET ultrastructure of a methanogen affiliated with the class Methanosuratincolia (formerly Verstraetearchaeota) within the phylum Thermoproteota. This is the first study demonstrating methanogenesis outside the Euryarchaeota.

In review. Krukenberg V, Kohtz AJ, Jay ZJ, Hatzenpichler R*. Methyl-reducing methanogenesis by a thermophilic culture of Korarchaeia​.
Cultivation and physiology of a thermophilic methanol-reducing methanogen affiliated with the archaeal class Korarchaeia. 

In review.Hug LA, Hatzenpichler R, Moraru C, Soares A, Meyer F, Heyder A, The Data Reuse Consortium, Probst AJ. A roadmap for fair reuse of public microbiome data. 

This article presents a roadmap to establish best practices for sequence data reuse, developed in consultation with a data consortium of 167 microbiome scientists. It introduces a Data Reuse Information tag (DRI) for public sequencing data, which will be associated with at least one Open Researcher and Contributor ID (ORCID) account.

42. Murali R, Pace LA, Sanford RA, Ward LM, Lynes MHatzenpichler R, Lingappa UF, Fischer WW, Gennis RB, Hemp J. Diversity and evolution of nitric oxide reduction. PNAS, 121 (26) e2316422121   PDF
​Proposes that previously uncharacterized heme-copper oxidoreductases perform nitric oxide reduction and demonstrates that an enzyme from Rhodothermus marinus, belonging to one of these families, does perform nitric oxide reduction.

41. Lee KS, Landry Z, Athar A, Alcolombri U, Ayutthaya PPN, Berry D, Bettignies P, Bisova K, Cheng J-X, Csucs G, Cui G, Garcia-Timermans C, Goda K, Hatzenpichler R, Henshaw R, Huang WE, Ivleva N, Kneipp J, Kubryk P, Lee TK, Locke A, Lee SS, Ma B, Martinez-Perez C, Min W, Müller O, Nielsen PH, Notingher I, Ozeki Y, Palatinszky M, Pereira FC, Pezzotti G, Popp J, Riva A, Sapers HM, Schlücker S, Taylor GT, Wagner M, Yin H, Zenobi R, Sarkans U, Stocker R. MicrobioRaman: an open-access web repository for microbiological Raman spectroscopy data. Nat Microbiol (2024)

​Presents the establishment of an open-access  web-based repository for microbiological Raman data.

40. Lynes MM, Jay ZJ, Kohtz AJ, Hatzenpichler R*. Methylotrophic methanogenesis in the Archaeoglobi revealed by cultivation of Ca. Methanoglobus hypatiae from a Yellowstone hot spring.  The ISME J (2024)  PDF
Via cultivation, genome-resolved metatranscriptomics, stable isotope tracing, and fluorescence and electron microscopy we demonstrate that the Archaeoglobi M. hypatiae is a methylotrophic methanogen that converts different methylamines to methane.

39. Murali R, Metcalfe KS, Yu H, Speth D, Wu F, Crémière A, Laso-Pèrez R, Malmstrom RM, Goudeau D, Woyke T, Hatzenpichler R, Chadwick GL, Orphan VJ. Physiological potential and evolutionary trajectories of syntrophic sulfate-reducing bacterial partners of anaerobic methanotrophic archaea.  PDF

Comparative genomics of four clades of syntrophic sulfate-reducing bacteria, demonstrating that they independently adapted to live in association with methanotrophic archaea.

38. Frates E, Spietz RL, Silverstein M, Girguis P, Hatzenpichler R, Marlow JJ. Natural and anthropogenic carbon input affect microbial activity in salt marsh sediment. Front Microbiol, accepted (2023)   PDF

Studies the effects of Spartina and diesel fuel addition on a salt marsh sediment microbiome using BONCAT-FACS coupled to amplicon gene sequencing of active cells.

37. Pavlopoulos GA, Baltoumas FA, Liu S, Selvitopi O, Nayfach S, Azad A, Call L, Camargo AP, Ivanova NN, Chen IM, Paez-Espino D, Karatzas E, Novel Metagenome Protein Families Consortium, Iliopoulos I, Konstantinidis K, Tiedje JM, Baker D, Ouzounis CA, Ovchinnikov S, Buluç A, Kyrpides NC. Discovery, diversity and distribution of functional dark matter through global metagenomics. Nature, accepted (2023)

The lab provided DNA samples for this global analyses of genetic dark matter.

36. Lynes M, Krukenberg V*, Jay ZJ, Kohtz AJ, Gobrogge C, Spietz RL, Hatzenpichler R*. Diversity and function of methyl-coenzyme M reductase-encoding archaea in Yellowstone hot springs revealed by metagenomics and mesocosm experiments. In review

Shows that diverse Methyl-coenzyme M reductase (Mcr) encoding archaea with the metabolic potential to produce methane from different precursors persist in diverse geothermal environments of Yellowstone National Park.   PDF   Download SOI datasets

35. Wiegand T, Wilkinson R, Santiago-Frangos A, Lynes M, Hatzenpichler R, Wiedenheft B. Functional and phylogenetic diversity of Cas10 proteins. The CRISPR J. DOI: 10.1089/crispr.2022.0085 (2023)   PDF
Uses computational and phylogenetic methods to analyze 2,014 Cas10 sequences from (meta)genomic datasets and functionally characterizes five representatives from three phylogenetically distinct clades.

34. Meadows V, Graham H, and workshop participants (including Hatzenpichler R). Community Report from the Biosignatures Standards of Evidence Workshop. arXiv:2210.14293 (2022).   PDF
Report on the outcomes of a a community-organized workshop on standards for life detection that was held on July 19-22, 2021.

​33. Kohtz AJ, Jay ZJ, Lynes M, Krukenberg V, Hatzenpichler R*. Culexarchaeia, a novel archaeal class of anaerobic generalists inhabiting geothermal environments. ISME Comm, (2022)  PDF   Download SOI
Describes the discovery of a new clade of archaea, Culexarchaeiea. Analyses of 10 metagenome-assembled genomes retrieved from five hot spring and two hydrothermal marine sediment samples reveals they are generalists with the potential for anaerobic methylotrophy.

32. Schaible GA, Kohtz AJ, Cliff J, Hatzenpichler R*​. Correlative SIP-FISH-SEM-Raman-NanoSIMS links identity, morphology, biochemistry, and physiology of environmental microbes​. ISME Comm, (2022)

PDF   Download SOI tables​​   EMSL press release
Develops a multi-modal correlative microscopy workflow and applies it to study multicellular magnetotactic bacteria from a salt marsh.

31. Reichart NJ, Bowers RM, Woyke T, Hatzenpichler R*. Metagenomes and metagenome-assembled genomes from substrate-amended hot spring sediment incubations. Microbiology Resource Announcements (2022)   PDF

Makes 74 medium and high quality MAGs from eight metagenomes obtained from hot spring mesocosm incubations publicly available.

30. Fremin BJ, Global Phage Small Open Reading Frame (GP-SmORF) Consortium, Bhatt AS, Kyrpides NC. Thousands of small, novel genes predicted in global phage genomes. Cell Reports, 39:12: 110984​ (2022)    PDF 

Study on predicting small genes in phage genomes. Our lab contributed DNA sequencing data to the project but was not involved in data analyses or interpretation.

29. Chadwick GL, Skennerton CT, Laso-Perez R, Leu AO, Speth DR, Yu H, Morgan-Lang C, Hatzenpichler R, Goudeau D, Malmstrom RR, Brazelton WJ, Woyke T, Hallam S, Tyson GW, Wegener G, Boetius A, Orphan VJ. Unique metabolic systems differentiate syntrophic methanotrophic archaea from methanogens. PLoS Biology 20: e3001508 (2022)   PDF

Determines genomic features that separate anaerobic methanotrophs (ANME) from methanogens and what differentiates ANME clades.

28. Krukenberg V, Reichart N, Spietz R, Hatzenpichler R*. Microbial community response to polysaccharide amendment in anoxic hydrothermal sediments of the Guaymas Basin. Front Microbiol doi:10.3389/fmicb.2021.763971 (2021)   PDF

Uses mesocosm incubations and BONCAT-FACS to ID microbes changing activity in response to HMW Corg amendment. Demonstrates that an initially minor but diverse population of Clostridia changes its protein synthesis activity in response to amendment.

27. Schmidt B, Johnson SS, Hoehler T, Graham H, Bowman J, Som S, Barge L, Cabrol N, Pavlov A, Pontefract A, Stockton A, Orcutt B, Nunn B, Foreman C, Stillman D, Shock E, Kenig F, Love G,  Bergmann K, Sobron P,  Mathies R, Hatzenpichler R, Yu S, Swingley W, Jones D, Lawrence J, Bryson F, Spiers E, Chivers C, Plattner T, Mullen A, Hanna A, Buffo J. Enabling Progress Towards Life Detection on NASA Missions. Planetary Science and Astrobiology Decadal Survey 2023-2032 white paper e-id. 260; Bulletin of the American Astronomical Society, 53 (4), e-id 260 (2021)   PDF

White paper on novel approaches for detecting life (as we know it and don't know it) on moons and planets in our solar system.

26. Marlow 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. Environ Microbiol, 23 (8), 4756-4777 (2021)   PDF

​BONCAT, resin embedding, fluorescence microscopy, electron microscopy, and energy dispersive X-ray spectroscopy are combined to reveal the spatial patterning of translationally active cells around specific mineral particles in heterogenous salt marsh sediment. 

25. Wang Q, Alowaifeer A, Kerner P, Balasubramanian N, Patterson A, Christian W, Tarver A, Dore JE, Hatzenpichler R, Bothner BB, McDermott TR. Aerobic bacterial methane synthesis. Proc Natl Acad Sci U.S.A., 118 (27) e2019229118 (2021)   PDF   MSU press release

Presents a new solution to the "methane paradox". Reports on the discovery of a single enzyme capable of generating methane from methylamine in a freshwater bacterium, and demonstrates that this capability to make methane is genetically transferrable to E. coli. 

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   Watch video: 'Behind the paper' & Nick's experience at the JGI

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 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 was  not involved in data analyses or interpretation.

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.