Physiological and genomic characterization of two novel marine thaumarchaeal strains indicates niche differentiation - PubMed (original) (raw)
Physiological and genomic characterization of two novel marine thaumarchaeal strains indicates niche differentiation
Barbara Bayer et al. ISME J. 2016 May.
Abstract
Ammonia-oxidizing Archaea (AOA) are ubiquitous throughout the oceanic water column; however, our knowledge on their physiological and ecological diversity in different oceanic regions is rather limited. Here, we report the cultivation and characterization of two novel Nitrosopumilus strains, originating from coastal surface waters of the Northern Adriatic Sea. The combined physiological and genomic information revealed that each strain exhibits different metabolic and functional traits, potentially reflecting contrasting life modes. Strain NF5 contains many chemotaxis-related genes and is able to express archaella, suggesting that it can sense and actively seek favorable microenvironments such as nutrient-rich particles. In contrast, strain D3C is non-motile and shows higher versatility in substrate utilization, being able to use urea as an alternative substrate in addition to ammonia. Furthermore, it encodes a divergent, second copy of the AmoB subunit of the key enzyme ammonia monooxygenase, which might have an additional catalytic function and suggests further metabolic versatility. However, the role of this gene requires further investigation. Our results provide evidence for functional diversity and metabolic versatility among phylogenetically closely related thaumarchaeal strains, and point toward adaptations to free-living versus particle-associated life styles and possible niche differentiation among AOA in marine ecosystems.
Figures
Figure 1
Phylogenetic tree of concatenated 16S–23S rRNA genes from cultivated Thaumarchaeota with sequenced genomes (16 organisms) showing the affiliation of strains D3C and NF5. Full-length gene sequences were aligned with MAFFT (L-INS-I method) based on Archaea-specific structurally accurate seed alignments (1474 and 3026 aligned positions for 16S and 23S rRNA genes, respectively), and unreliable positions were filtered from the resulting alignments with TCS before concatenation (4443 aligned positions in the concatenated alignment). The tree was calculated by maximum likelihood with IQ-Tree based on the GTR+I+Γ4 model, with ultrafast bootstrap (UFBoot) and SH-aLRT support values inferred from 1000 replicates each (see Supplementary materials and methods for details). Support values ⩾85% are represented on the respective branches by semi-circles color-coded as indicated on the figure.
Figure 2
Transmission electron microscopy (a, b) and scanning electron microscopy (c, d) images of strains NF5 (left) and D3C (right).
Figure 3
Typical growth curve of strains D3C (a) and NF5 (b) in medium containing 1 m
m
NH4Cl. Triangles: NH4+ concentrations, full circles: NO2− concentrations, open circles: cell abundances. Error bars represent standard deviations of measurements from triplicate cultures.
Figure 4
Growth of strains D3C and NF5 in medium supplemented with 0.5 m
m
urea. Open circles: cell abundances, full circles: NO2− production. Error bars represent standard deviations of measurements from triplicate cultures.
Similar articles
- Nitrosopumilus adriaticus sp. nov. and Nitrosopumilus piranensis sp. nov., two ammonia-oxidizing archaea from the Adriatic Sea and members of the class Nitrososphaeria.
Bayer B, Vojvoda J, Reinthaler T, Reyes C, Pinto M, Herndl GJ. Bayer B, et al. Int J Syst Evol Microbiol. 2019 Jul;69(7):1892-1902. doi: 10.1099/ijsem.0.003360. Epub 2019 Apr 2. Int J Syst Evol Microbiol. 2019. PMID: 30938665 - Genome-enabled transcriptomics reveals archaeal populations that drive nitrification in a deep-sea hydrothermal plume.
Baker BJ, Lesniewski RA, Dick GJ. Baker BJ, et al. ISME J. 2012 Dec;6(12):2269-79. doi: 10.1038/ismej.2012.64. Epub 2012 Jun 14. ISME J. 2012. PMID: 22695863 Free PMC article. - Genomic adaptation to eutrophication of ammonia-oxidizing archaea in the Pearl River estuary.
Zou D, Li Y, Kao SJ, Liu H, Li M. Zou D, et al. Environ Microbiol. 2019 Jul;21(7):2320-2332. doi: 10.1111/1462-2920.14613. Epub 2019 Apr 14. Environ Microbiol. 2019. PMID: 30924222 - Environmental factors shaping the ecological niches of ammonia-oxidizing archaea.
Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W. Erguder TH, et al. FEMS Microbiol Rev. 2009 Sep;33(5):855-69. doi: 10.1111/j.1574-6976.2009.00179.x. Epub 2009 Apr 21. FEMS Microbiol Rev. 2009. PMID: 19453522 Review. - Physiology and diversity of ammonia-oxidizing archaea.
Stahl DA, de la Torre JR. Stahl DA, et al. Annu Rev Microbiol. 2012;66:83-101. doi: 10.1146/annurev-micro-092611-150128. Annu Rev Microbiol. 2012. PMID: 22994489 Review.
Cited by
- Metabolite release by nitrifiers facilitates metabolic interactions in the ocean.
Bayer B, Liu S, Louie K, Northen TR, Wagner M, Daims H, Carlson CA, Santoro AE. Bayer B, et al. ISME J. 2024 Jan 8;18(1):wrae172. doi: 10.1093/ismejo/wrae172. ISME J. 2024. PMID: 39244747 Free PMC article. - Ammonia-oxidizing bacteria and archaea exhibit differential nitrogen source preferences.
Qin W, Wei SP, Zheng Y, Choi E, Li X, Johnston J, Wan X, Abrahamson B, Flinkstrom Z, Wang B, Li H, Hou L, Tao Q, Chlouber WW, Sun X, Wells M, Ngo L, Hunt KA, Urakawa H, Tao X, Wang D, Yan X, Wang D, Pan C, Weber PK, Jiang J, Zhou J, Zhang Y, Stahl DA, Ward BB, Mayali X, Martens-Habbena W, Winkler MH. Qin W, et al. Nat Microbiol. 2024 Feb;9(2):524-536. doi: 10.1038/s41564-023-01593-7. Epub 2024 Jan 31. Nat Microbiol. 2024. PMID: 38297167 - Increased prokaryotic diversity in the Red Sea deep scattering layer.
Huete-Stauffer TM, Logares R, Ansari MI, Røstad A, Calleja ML, Morán XAG. Huete-Stauffer TM, et al. Environ Microbiome. 2023 Dec 14;18(1):87. doi: 10.1186/s40793-023-00542-5. Environ Microbiome. 2023. PMID: 38098078 Free PMC article. - Nitrification and beyond: metabolic versatility of ammonia oxidising archaea.
Wright CL, Lehtovirta-Morley LE. Wright CL, et al. ISME J. 2023 Sep;17(9):1358-1368. doi: 10.1038/s41396-023-01467-0. Epub 2023 Jul 14. ISME J. 2023. PMID: 37452095 Free PMC article. Review. - A comprehensive history of motility and Archaellation in Archaea.
Jarrell KF, Albers SV, Machado JNS. Jarrell KF, et al. FEMS Microbes. 2021 Apr 8;2:xtab002. doi: 10.1093/femsmc/xtab002. eCollection 2021. FEMS Microbes. 2021. PMID: 37334237 Free PMC article.
References
- Abraham W-R, Rohde M. (2014). The family Hyphomonadacaea. In: The Prokaryotes. Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds). Springer-Verlag: Berlin, Heidelberg, 4: 283–297.
- Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. (1990). Basic local alignment search tool. J Mol Biol 215: 403–410. - PubMed
- Aoshima M, Ishii M, Igarashi Y. (2004. a). A novel enzyme, citryl-CoA synthetase, catalysing the first step of the citrate cleavage reaction in Hydrogenobacter thermophilus TK-6. Mol Microbiol 52: 751–761. - PubMed
- Aoshima M, Ishii M, Igarashi Y. (2004. b). A novel enzyme, citryl-CoA lyase, catalysing the second step of the citrate cleavage reaction in Hydrogenobacter thermophilus TK-6. Mol Microbiol 52: 763–770. - PubMed
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources
Molecular Biology Databases