Constraining the composition and quantity of organic matter used by abundant marine Thaumarchaeota.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
03 2023
03 2023
Historique:
received:
23
09
2022
accepted:
27
11
2022
pubmed:
9
12
2022
medline:
15
3
2023
entrez:
8
12
2022
Statut:
ppublish
Résumé
Marine Group I (MGI) Thaumarchaeota were originally described as chemoautotrophic nitrifiers, but molecular and isotopic evidence suggests heterotrophic and/or mixotrophic capabilities. Here, we investigated the quantity and composition of organic matter assimilated by individual, uncultured MGI cells from the Pacific Ocean to constrain their potential for mixotrophy and heterotrophy. We observed that most MGI cells did not assimilate carbon from any organic substrate provided (glucose, pyruvate, oxaloacetate, protein, urea, and amino acids). The minority of MGI cells that did assimilate it did so exclusively from nitrogenous substrates (urea, 15% of MGI and amino acids, 36% of MGI), and only as an auxiliary carbon source (<20% of that subset's total cellular carbon was derived from those substrates). At the population level, MGI assimilation of organic carbon comprised just 0.5%-11% of total biomass carbon. We observed extensive assimilation of inorganic carbon and urea- and amino acid-derived nitrogen (equal to that from ammonium), consistent with metagenomic and metatranscriptomic analyses performed here and previously showing a widespread potential for MGI to perform autotrophy and transport and degrade organic nitrogen. Our results constrain the quantity and composition of organic matter used by MGI and suggest they use it primarily to meet nitrogen demands for anabolism and nitrification.
Identifiants
pubmed: 36478085
doi: 10.1111/1462-2920.16299
doi:
Substances chimiques
Carbon
7440-44-0
Amino Acids
0
Urea
8W8T17847W
Nitrogen
N762921K75
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
689-704Informations de copyright
© 2022 Applied Microbiology International and John Wiley & Sons Ltd.
Références
Ahlgren, N.A., Chen, Y., Needham, D.M., Parada, A.E., Sachdeva, R., Trinh, V. et al. (2017) Genome and epigenome of a novel marine Thaumarchaeota strain suggest viral infection, phosphorothioation DNA modification, and multiple restriction systems. ISME Journal,19(6), 2434-2452.
Alonso-Sáez, L., Sánchez, O., Gasol, J.M., Balagué, V. & Pedrós-Alio, C. (2008) Winter-to-summer changes in the composition and single-cell activity of near-surface Arctic prokaryotes. Environmental Microbiology, 10, 2444-2454.
Alonso-Sáez, L., Waller, A.S., Mende, D.R., Bakker, K., Farnelid, H., Yager, P.L. et al. (2012) Role for urea in nitrification by polar marine Archaea. Proceedings of the National Academy of Sciences of the United States of America, 109, 17989-17994.
Amann, R.I., Binder, B.J., Olson, R.J., Chisholm, S.W., Devereux, R. & Stahl, D.A. (1990) Combination of 16 S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Applied and Environmental Microbiology, 56, 1919-1925.
Aylward, F.O. & Santoro, A.E. (2020) Heterotrophic Thaumarchaeota with ultrasmall genomes are widespread in the ocean. mSystems, 5, e00415-e00420.
Baker, B.J., Lesniewski, R.A. & Dick, G.J. (2012) Genome-enabled transcriptomics reveals archaeal populations that drive nitrification in a deep-sea hydrothermal plume. The ISME Journal, 6, 2269-2279.
Bayer, B., Hansman, R.L., Bittner, M.J., Noriega-Ortega, B.E., Niggemann, J., Dittmar, T. et al. (2019) Ammonia-oxidizing archaea release a suite of organic compounds potentially fueling prokaryotic heterotrophy in the ocean. Environmental Microbiology, 21, 4062-4075.
Bayer, B., McBeain, K., Carlson, C.A. & Santoro, A.E. (2022) Carbon content, carbon fixation yield and dissolved organic carbon release from diverse marine nitrifiers. Limnology and Oceanography.
Bayer, B., Vojvoda, J., Offre, P., Alves, R.J.E., Elisabeth, N.H., Garcia, J.A.L. et al. (2016) Physiological and genomic characterization of two novel marine thaumarchaeal strains indicates niche differentiation. ISME Journal, 10, 1051-1063.
Beman, J.M., Chow, C.-E., King, A.L., Feng, Y., Fuhrman, J.A., Andersson, A. et al. (2011) Global declines in oceanic nitrification rates as a consequence of ocean acidification. Proceedings of the National Academy of Sciences of the United States of America, 108, 208-213.
Beman, J.M., Popp, B.N. & Francis, C.A. (2008) Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. The ISME Journal, 2, 429-441.
Benson, D.A., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J. & Wheeler, D.L. (2005) GenBank. Nucleic Acids Research, 33, 34-38.
Berg, J.M., Tymoczko, J.L. & Stryer, L. (2002) The citric acid cycle. In: Biochemistry. New York, NY: W.H. Freeman.
Bolger, A.M., Lohse, M. & Usadel, B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114-2120.
Bowers, R.M., Kyrpides, N.C., Stepanauskas, R., Harmon-Smith, M., Doud, D., Reddy, T.B.K. et al. (2017) Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nature Biotechnology, 35, 725-731.
Buchfink, B., Xie, C. & Huson, D.H. (2015) Fast and sensitive protein alignment using DIAMOND. Nature Methods, 12, 59-60.
Burton, S.A.Q. & Prosser, J.I. (2001) Autotrophic ammonia oxidation at low pH through urea hydrolysis. Applied and Environmental Microbiology, 67, 2952-2957.
Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K. et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7, 335-336.
Carini, P., Dupont, C.L. & Santoro, A.E. (2018) Patterns of thaumarchaeal gene expression in culture and diverse marine environments. Environmental Microbiology, 20, 2112-2124.
Damashek, J., Bayer, B., Herndl, G.J., Wallsgrove, N.J., Allen, T., Popp, B.N. et al. (2021) Limited accessibility of nitrogen supplied as amino acids, amides, and amines as energy sources for marine Thaumarchaeota. bioRxiv, 2021.07.22.453390.
Damashek, J., Tolar, B.B., Liu, Q., Okotie-Oyekan, A.O., Wallsgrove, N.J., Popp, B.N. et al. (2019) Microbial oxidation of nitrogen supplied as selected organic nitrogen compounds in the South Atlantic Bight. Limnology and Oceanography, 64, 982-995.
Dekas, A.E. & Orphan, V.J. (2011) Identification of diazotrophic microorganisms in marine sediment via fluorescence In situ hybridization coupled to nanoscale secondary ion mass spectrometry (FISH-NanoSIMS). In: Klotz, M.G. (Ed.) Methods in enzymology. Cambridge, MA: Academic Press, pp. 281-305.
Dekas, A.E., Parada, A.E., Mayali, X., Fuhrman, J.A., Wollard, J., Weber, P.K. et al. (2019) Characterizing chemoautotrophy and heterotrophy in marine archaea and bacteria with single-cell multi-isotope NanoSIP. Frontiers in Microbiology, 10, 2682.
Dugdale, R.C. & Goering, J.J. (1967) Uptake of new and regenerated forms of nitrogen in primary productivity. Limnology and Oceanography, 12(2), 196-206. Available from: https://doi.org/10.4319/lo.1967.12.2.0196
Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics, 28(23), 3150-3152. Available from: https://doi.org/10.1093/bioinformatics/bts565
Edgar, R.C. (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics (Oxford, England), 26, 2460-2461.
Eren, A.M., Kiefl, E., Shaiber, A., Veseli, I., Miller, S.E., Schechter, M.S. et al. (2021) Community-led, integrated, reproducible multi-omics with anvi'o. Nature Microbiology, 6, 3-6.
Eren, A.M., Vineis, J.H., Morrison, H.G. & Sogin, M.L. (2013) A filtering method to generate high quality short reads using Illumina paired-end technology. PLoS ONE, 8, 6-11.
Fry, B., Hopkinson, C.S., Nolin, A. & Wainright, S.C. (1998) 13C/12C composition of marine dissolved organic carbon. Chemical Geology, 152, 113-118.
Hatch, M.D. & Heldt, H.W. (1985) Synthesis, storage, and stability of [4-14C]oxaloacetic acid. Analytical Biochemistry, 145, 393-397.
Herndl, G.J., Reinthaler, T., Teira, E., van Aken, H.M., Veth, C., Pernthaler, A. et al. (2005) Contribution of archaea to total prokaryotic production in the deep Atlantic Ocean. Applied and Environmental Microbiology, 71, 2303-2309.
Holmes, R.M., Aminot, A., Kerouel, R., Hooker, B.A. & Peterson, B.J. (1999) A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Canadian Journal of Fisheries and Aquatic Sciences, 56, 1801-1808.
Hug, L.A., Thomas, B.C., Sharon, I., Brown, C.T., Sharma, R., Hettich, R.L. et al. (2016) Critical biogeochemical functions in the subsurface are associated with bacteria from new phyla and little studied lineages: N- and C-cycling organisms in the subsurface. Environmental Microbiology, 18, 159-173.
Ingalls, A.E., Shah, S.R., Hansman, R.L., Aluwihare, L.I., Santos, G.M., Druffel, E.R.M. et al. (2006) Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. Proceedings of the National Academy of Sciences of the United States of America, 103, 6442-6447.
Karner, M.B., DeLong, E.F. & Karl, D.M. (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature, 409, 507-510.
Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772-780.
Kim, J.-G., Park, S.-J., Sinninghe Damsté, J.S., Schouten, S., Rijpstra, W.I.C., Jung, M.-Y. et al. (2016) Hydrogen peroxide detoxification is a key mechanism for growth of ammonia-oxidizing archaea. Proceedings of the National Academy of Sciences of the United States of America, 113, 7888-7893.
Kirchman, D.L., Elifantz, H., Dittel, A.I., Malmstrom, R.R. & Cottrell, M.T. (2007) Standing stocks and activity of Archaea and Bacteria in the Western Arctic Ocean. Limnology and Oceanography, 52, 495-507.
Kitzinger, K., Marchant, H.K., Bristow, L.A., Herbold, C.W., Padilla, C.C., Kidane, A.T. et al. (2020) Single cell analyses reveal contrasting life strategies of the two main nitrifiers in the ocean. Nature Communications, 11, 767.
Kitzinger, K., Padilla, C.C., Marchant, H.K., Hach, P.F., Herbold, C.W., Kidane, A.T. et al. (2019) Cyanate and urea are substrates for nitrification by Thaumarchaeota in the marine environment. Nature Microbiology, 4, 234-243.
Konstantinidis, K.T., Braff, J., Karl, D.M. & DeLong, E.F. (2009) Comparative metagenomic analysis of a microbial community residing at a depth of 4000 meters at station ALOHA in the North Pacific subtropical gyre. Applied and Environmental Microbiology, 75, 5345-5355.
Krüger, M., Wolters, H., Gehre, M., Joye, S.B. & Richnow, H.H. (2008) Tracing the slow growth of anaerobic methane-oxidizing communities by (15)N-labelling techniques. FEMS Microbiology Ecology, 63, 401-411.
Langmead, B. & Salzberg, S.L. (2012) Fast gapped-read alignment with Bowtie 2. Nature Methods, 9, 357-359.
Legin, A.A., Schintlmeister, A., Jakupec, M.A., Galanski, M., Lichtscheidl, I., Wagner, M. et al. (2014) NanoSIMS combined with fluorescence microscopy as a tool for subcellular imaging of isotopically labeled platinum-based anticancer drugs. Chemical Science, 5, 3135-3143.
Letunic, I. & Bork, P. (2019) Interactive Tree of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Research, 47, 256-259.
Li, D., Luo, R., Liu, C.M., Leung, C.M., Ting, H.F., Sadakane, K. et al. (2016) MEGAHIT v1.0: a fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods, 102, 3-11.
Li, M., Baker, B.J., Anantharaman, K., Jain, S., Breier, J.A. & Dick, G.J. (2015) Genomic and transcriptomic evidence for scavenging of diverse organic compounds by widespread deep-sea archaea. Nature Communications, 6, 8933.
Luo, H., Tolar, B.B., Swan, B.K., Zhang, C.L., Stepanauskas, R., Ann Moran, M. et al. (2014) Single-cell genomics shedding light on marine Thaumarchaeota diversification. The ISME Journal, 8, 732-736.
Mahé, F., Rognes, T., Quince, C., de Vargas, C. & Dunthorn, M. (2014) Swarm: robust and fast clustering method for amplicon-based studies. PeerJ, 2, e593.
Martens-Habbena, W., Berube, P.M., Urakawa, H., de la Torre, J.R. & Stahl, D.A. (2009) Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature, 461, 976-979.
Mayali, X., Weber, P.K. & Pett-Ridge, J. (2013) Taxon-specific C/N relative use efficiency for amino acids in an estuarine community. FEMS Microbiology Ecology, 83, 402-412.
McIlvin, M.R. & Casciotti, K.L. (2011) Technical updates to the bacterial method for nitrate isotopic analyses. Analytical Chemistry, 83(5), 1850-1856. Available from: https://doi.org/10.1021/ac1028984
Meyer, N.R., Fortney, J.L. & Dekas, A.E. (2021) NanoSIMS sample preparation decreases isotope enrichment: magnitude, variability and implications for single-cell rates of microbial activity. Environmental Microbiology, 23, 81-98.
Mirarab, S., Nguyen, N. & Warnow, T. (2012) (2011) SEPP: SATé-enabled phylogenetic placement. In: Biocomputing. Kohala Coast, Hawaii, USA: World Scientific, pp. 247-258.
Mobley, H.L.T., Island, M.D. & Hausinger, R.P. (1995) Molecular biology of microbial ureases. Microbiological Reviews, 59, 451-480.
Musat, N., Musat, F., Weber, P.K. & Pett-Ridge, J. (2016) Tracking microbial interactions with NanoSIMS. Current Opinion in Biotechnology, 41, 114-121.
Mußmann, M., Brito, I., Pitcher, A., Sinninghe Damste, J.S., Hatzenpichler, R., Richter, A. et al. (2011) Thaumarchaeotes abundant in refinery nitrifying sludges express AmoA but are not obligate autotrophic ammonia oxidizers. Proceedings of the National Academy of Sciences, 108(40), 16771-16776. Available from: https://doi.org/10.1073/pnas.1106427108
Musat, N., Stryhanyuk, H., Bombach, P., Adrian, L., Audinot, J.N. & Richnow, H.H. (2014) The effect of FISH and CARD-FISH on the isotopic composition of 13C- and 15N-labeled Pseudomonas putida cells measured by nanoSIMS. Systematic and Applied Microbiology, 37, 267-276.
Nagata, T. (2008) Organic matter-bacteria interactions in seawater. In: Kirchman, D.L. (Ed.) Microbial ecology of the oceans. Hoboken, NJ: John Wiley & Sons, Inc., pp. 207-241.
Orphan, V.J., Turk, K.A., Green, A.M. & House, C.H. (2009) Patterns of 15N assimilation and growth of methanotrophic ANME-2 archaea and sulfate-reducing bacteria within structured syntrophic consortia revealed by FISH-SIMS. Environmental Microbiology, 11, 1777-1791.
Ouverney, C.C. & Fuhrman, J.A. (2000) Marine planktonic archaea take up amino acids. Applied and Environmental Microbiology, 66, 4829-4833.
Parada, A.E. & Fuhrman, J.A. (2017) Marine archaeal dynamics and interactions with the microbial community over 5 years from surface to seafloor. ISME Journal, 11, 2510-2525.
Parada, A.E., Needham, D.M. & Fuhrman, J.A. (2016) Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environmental Microbiology, 18, 1403-1414.
Parks, D.H., Chuvochina, M., Waite, D.W., Rinke, C., Skarshewski, A., Chaumeil, P.-A. et al. (2018) A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nature Biotechnology, 36, 996-1004.
Parks, D.H., Imelfort, M., Skennerton, C.T., Hugenholtz, P. & Tyson, G.W. (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Research, 25, 1043-1055.
Parsons, T.R., Maita, Y. & Lalli, C.M. (1984) A manual of chemical and biological methods for seawater analysis. Elmsford, NY: Pergamon Press Inc.
Pearson, A., McNichol, A.P., Benitez-Nelson, B.C., Hayes, J.M. & Eglinton, T.I. (2001) Origins of lipid biomarkers in Santa Monica Basin surface sediment: a case study using compound-specific Δ14C analysis. Geochimica et Cosmochimica Acta, 65, 3123-3137.
Pernthaler, A. & Pernthaler, J. (2007) Fluorescence in situ hybridization for the identification of environmental microbes. Methods in Molecular Biology, 353, 153-164.
Pett-Ridge, J. & Weber, P.K. (2022) NanoSIP: NanoSIMS applications for microbial biology. Methods in Molecular Biology, 2349, 91-136.
Popa, R., Weber, P.K., Pett-Ridge, J., Finzi, J.A., Fallon, S.J., Hutcheon, I.D. et al. (2007) Carbon and nitrogen fixation and metabolite exchange in and between individual cells of Anabaena oscillarioides. ISME Journal, 1, 354-360.
Price, M.N., Dehal, P.S. & Arkin, A.P. (2010) FastTree 2 - approximately maximum-likelihood trees for large alignments. PLoS ONE, 5, e9490.
Pritchard, L., Glover, R.H., Humphris, S., Elphinstone, J.G. & Toth, I.K. (2016) Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Analytical Methods, 8, 12-24.
Qin, W., Amin, S.A., Martens-Habbena, W., Walker, C.B., Urakawa, H., Devol, A.H. et al. (2014) Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation. Proceedings of the National Academy of Sciences of the United States of America, 111, 12504-12,509.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P. et al. (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research, 41, D590-D596.
R Core Team. (2015) R: a language and environment for statistical computing.
Reji, L. & Francis, C.A. (2020) Metagenome-assembled genomes reveal unique metabolic adaptations of a basal marine Thaumarchaeota lineage. ISME Journal., 14, 2105-2115.
Rinke, C., Chuvochina, M., Mussig, A.J., Chaumeil, P.-A., Davín, A.A., Waite, D.W. et al. (2021) A standardized archaeal taxonomy for the Genome Taxonomy Database. Nature Microbiology, 6, 946-959.
Rosman, K.J.R. & Taylor, P.D.P. (1998) Isotopic compositions of the elements 1997 (Technical Report). Pure and Applied Chemistry, 70, 217-235.
Santoro, A.E. & Casciotti, K.L. (2011) Enrichment and characterization of ammonia-oxidizing archaea from the open ocean: phylogeny, physiology and stable isotope fractionation. The ISME journal, 5, 1796-1808.
Santoro, A.E., Dupont, C.L., Richter, R.A., Craig, M.T., Carini, P., McIlvin, M.R. et al. (2015) Genomic and proteomic characterization of “Candidatus Nitrosopelagicus brevis”: an ammonia-oxidizing archaeon from the open ocean. Proceedings of the National Academy of Sciences of the United States of America, 112, 1173-1178.
Schouten, S., Hopmans, E.C., Pancost, R.D. & Damste, J.S.S. (2000) Widespread occurrence of structurally diverse tetraether membrane lipids: evidence for the ubiquitous presence of low-temperature relatives of hyperthermophiles. Proceedings of the National Academy of Sciences of the United States of America, 97, 14421-14426.
Seemann, T. (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics (Oxford, England), 30, 2068-2069.
Segata, N., Börnigen, D., Morgan, X.C. & Huttenhower, C. (2013) PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nature Communications, 4, 2304.
Seyler, L.M., McGuinness, L.M. & Kerkhof, L.J. (2014) Crenarchaeal heterotrophy in salt marsh sediments. ISME Journal, 8, 1534-1543.
Seyler, L.M., McGuinness, L.R., Gilbert, J.A., Biddle, J.F., Gong, D. & Kerkhof, L.J. (2018) Discerning autotrophy, mixotrophy, and heterotrophy in marine TACK archaea from the North Atlantic. FEMS Microbiology Ecology, 94(3), fiy014.
Sommer, D.D., Delcher, A.L., Salzberg, S.L. & Pop, M. (2007) Minimus: a fast, lightweight genome assembler. BMC Bioinformatics, 8(1). Available from: https://doi.org/10.1186/1471-2105-8-64
Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312-1313.
Swan, B.K., Chaffin, M.D., Martinez-Garcia, M., Morrison, H.G., Field, E.K., Poulton, N.J. et al. (2014) Genomic and metabolic diversity of Marine Group I Thaumarchaeota in the mesopelagic of two subtropical gyres. PLoS ONE, 9, e95380.
Teira, E., Lebaron, P., van Aken, H.M. & Herndl, G.J. (2006) Distribution and activity of Bacteria and Archaea in the deep water masses of the North Atlantic. Limnology and Oceanography, 51, 2131-2144.
Teira, E., Reinthaler, T., Pernthaler, A., Pernthaler, J. & Herndl, G.J. (2004) Combining catalyzed reporter deposition-fluorescence in situ hybridization and microautoradiography to detect substrate utilization by bacteria and archaea in the deep ocean. Applied and Environmental Microbiology, 70, 4411-4414.
Teira, E., van Aken, H., Veth, C. & Herndl, G.J. (2006) Archaeal uptake of enantiomeric amino acids in the meso- and bathypelagic waters of the North Atlantic. Limnology and Oceanography, 51, 60-69.
Tolar, B.B., Wallsgrove, N.J., Popp, B.N. & Hollibaugh, J.T. (2017) Oxidation of urea-derived nitrogen by thaumarchaeota-dominated marine nitrifying communities. Environmental Microbiology, 19, 4838-4850.
Tully, B.J., Nelson, W.C. & Heidelberg, J.F. (2012) Metagenomic analysis of a complex marine planktonic thaumarchaeal community from the Gulf of Maine. Environmental Microbiology, 14, 254-267.
Varela, M.M., van Aken, H.M., Sintes, E., Reinthaler, T. & Herndl, G.J. (2011) Contribution of Crenarchaeota and Bacteria to autotrophy in the North Atlantic interior. Environmental Microbiology, 13, 1524-1533.
Walker, C.B., de la Torré, J.R., Klotz, M.G., Urakawa, H., Pinel, N., Arp, D.J. et al. (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proceedings of the National Academy of Sciences of the United States of America, 107, 8818-8823.
Wickham, H. (2016) ggplot2: Elegant graphics for data analysis. New York, NY: Springer-Verlag.
Woebken, D., Burow, L.C., Behnam, F., Mayali, X., Schintlmeister, A., Fleming, E.D. et al. (2015) Revisiting N2 fixation in Guerrero Negro intertidal microbial mats with a functional single-cell approach. ISME J, 9, 485-496.
Zhong, H., Lehtovirta-Morley, L., Liu, J., Zheng, Y., Lin, H., Song, D. et al. (2020) Novel insights into the Thaumarchaeota in the deepest oceans: their metabolism and potential adaptation mechanisms. Microbiome, 8, 78.