Autotrophic ammonia oxidation in a deep-sea hydrothermal plume

Lam, Phyllis; Cowen, James P.; Jones, Ronald D.

doi:10.1016/s0168-6496(03)00256-3

Cited by 84 publications

(101 citation statements)

References 86 publications

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“…Hydrothermal inputs into the deep GB lead to ammonium concentrations of 0.2-3 mM in plumes (Lam, 2004), which spans the range proposed to delineate niches of AOA and AOB (MartensHabbena et al, 2009). We found that transcripts of the MGI genes encoding ammonia monooxygenase (amoA) and an ammonium transporter were among the most abundant protein-coding transcripts in the deep GB microbial community (total of 405 and 1713 transcripts, respectively) and were more abundant in plume samples compared with the background (Figure 3).…”

Section: Resultsmentioning

confidence: 71%

“…As a result, ammonium concentrations in the GB end-member fluids (10.3-15.6 mM) (Von Damm et al, 1985) are considerably higher than unsedimented ridge discharge fluids (o0.01 mM; Lilley et al, 1993). These hydrothermal inputs contribute to ammonium concentrations of up to 3 mM in GB deep waters (1800-2000 m depth; Lam, 2004). Gene-based surveys have shown that the MGI dominate the GB plume archaeal community Tebo, 2010, Lesniewski et al, 2012), and that MGI are more abundant in plumes than background seawater in the deep Indian Ocean and Okinawa Trough (Takai et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

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Genome-enabled transcriptomics reveals archaeal populations that drive nitrification in a deep-sea hydrothermal plume

2012

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Ammonia-oxidizing Archaea (AOA) are among the most abundant microorganisms in the oceans and have crucial roles in biogeochemical cycling of nitrogen and carbon. To better understand AOA inhabiting the deep sea, we obtained community genomic and transcriptomic data from ammonium-rich hydrothermal plumes in the Guaymas Basin (GB) and from surrounding deep waters of the Gulf of California. Among the most abundant and active lineages in the sequence data were marine group I (MGI) Archaea related to the cultured autotrophic ammonia-oxidizer, Nitrosopumilus maritimus. Assembly of MGI genomic fragments yielded 2.9 Mb of sequence containing seven 16S rRNA genes (95.4–98.4% similar to N. maritimus), including two near-complete genomes and several lower-abundance variants. Equal copy numbers of MGI 16S rRNA genes and ammonia monooxygenase genes and transcription of ammonia oxidation genes indicates that all of these genotypes actively oxidize ammonia. De novo genomic assembly revealed the functional potential of MGI populations and enhanced interpretation of metatranscriptomic data. Physiological distinction from N. maritimus is evident in the transcription of novel genes, including genes for urea utilization, suggesting an alternative source of ammonia. We were also able to determine which genotypes are most active in the plume. Transcripts involved in nitrification were more prominent in the plume and were among the most abundant transcripts in the community. These unique data sets reveal populations of deep-sea AOA thriving in the ammonium-rich GB that are related to surface types, but with key genomic and physiological differences.

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Section: Resultsmentioning

confidence: 71%

Section: Introductionmentioning

confidence: 99%

Genome-enabled transcriptomics reveals archaeal populations that drive nitrification in a deep-sea hydrothermal plume

2012

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“…In contrast, the archaeal community in Movile Cave showed some similarity to deep-sea hydrothermal vent environments (Takai and Horikoshi, 1999), but differed from these in that no 16S rRNA sequences related to known ammonia-oxidizing archaea were found in our study, and Nitrosomonas spp. were probably the major nitrifiers in Movile Cave, whereas it has been suggested that ammoniaoxidizing Crenarchaea, rather than their bacterial counterparts, are the major nitrifiers in deep-sea vents (Lam et al, 2004;Nakagawa and Takai, 2008). Although it is possible that the clone library had bias because of the imperfect 16S rRNA primers for archaea, as well as bias during SIP incubations, our results imply that bacterial chemolithotrophs are probably the dominant primary producers in Movile Cave.…”

Section: Sulfur/ammonia-oxidizing Bacteria In Movile Cavementioning

confidence: 60%

Life without light: microbial diversity and evidence of sulfur- and ammonium-based chemolithotrophy in Movile Cave

et al. 2009

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Microbial diversity in Movile Cave (Romania) was studied using bacterial and archaeal 16S rRNA gene sequence and functional gene analyses, including ribulose-1,5-bisphosphate carboxylase/ oxygenase (RuBisCO), soxB (sulfate thioesterase/thiohydrolase) and amoA (ammonia monooxygenase). Sulfur oxidizers from both Gammaproteobacteria and Betaproteobacteria were detected in 16S rRNA, soxB and RuBisCO gene libraries. DNA-based stable-isotope probing analyses using 13 C-bicarbonate showed that Thiobacillus spp. were most active in assimilating CO 2 and also implied that ammonia and nitrite oxidizers were active during incubations. Nitrosomonas spp. were detected in both 16S rRNA and amoA gene libraries from the 'heavy' DNA and sequences related to nitriteoxidizing bacteria Nitrospira and Candidatus 'Nitrotoga' were also detected in the 'heavy' DNA, which suggests that ammonia/nitrite oxidation may be another major primary production process in this unique ecosystem. A significant number of sequences associated with known methylotrophs from the Betaproteobacteria were obtained, including Methylotenera, Methylophilus and Methylovorus, supporting the view that cycling of one-carbon compounds may be an important process within Movile Cave. Other sequences detected in the bacterial 16S rRNA clone library included Verrucomicrobia, Firmicutes, Bacteroidetes, alphaproteobacterial Rhodobacterales and gammaproteobacterial Xanthomonadales. Archaeal 16S rRNA sequences retrieved were restricted within two groups, namely the Deep-sea Hydrothermal Vent Euryarchaeota group and the Miscellaneous Crenarchaeotic group. No sequences related to known sulfur-oxidizing archaea, ammonia-oxidizing archaea, methanogens or anaerobic methane-oxidizing archaea were detected in this clone library. The results provided molecular biological evidence to support the hypothesis that Movile Cave is driven by chemolithoautotrophy, mainly through sulfur oxidation by sulfur-oxidizing bacteria and reveal that ammonia-and nitrite-oxidizing bacteria may also be major primary producers in Movile Cave.

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“…High ammonium and nitrate concentration can be found in sediment-hosted hydrothermal fields, such as the Guaymas Basin and Okinawa Trough Backarc Basin, as well as the Endeavor segment of the Juan de Fuca Ridge (Ishibashi et al, 1995;Mehta et al, 2003). It has been demonstrated that ammonium is rapidly consumed by chemoautotrophs in the hydrothermal plume of vents on the Juan de Fuca Ridge (Lam et al, 2004). However, we did not find genes encoding for ammonia monooxygenase (amoA), a key enzyme for ammonia oxidization, in the metagenome.…”

Section: Nitrogen Metabolismmentioning

confidence: 99%

Comparative metagenomics of microbial communities inhabiting deep-sea hydrothermal vent chimneys with contrasting chemistries

Xie

Wang

Guo³

et al. 2010

The ISME Journal

156

131

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Deep-sea hydrothermal vent chimneys harbor a high diversity of largely unknown microorganisms. Although the phylogenetic diversity of these microorganisms has been described previously, the adaptation and metabolic potential of the microbial communities is only beginning to be revealed. A pyrosequencing approach was used to directly obtain sequences from a fosmid library constructed from a black smoker chimney 4143-1 in the Mothra hydrothermal vent field at the Juan de Fuca Ridge. A total of 308 034 reads with an average sequence length of 227 bp were generated. Comparative genomic analyses of metagenomes from a variety of environments by two-way clustering of samples and functional gene categories demonstrated that the 4143-1 metagenome clustered most closely with that from a carbonate chimney from Lost City. Both are highly enriched in genes for mismatch repair and homologous recombination, suggesting that the microbial communities have evolved extensive DNA repair systems to cope with the extreme conditions that have potential deleterious effects on the genomes. As previously reported for the Lost City microbiome, the metagenome of chimney 4143-1 exhibited a high proportion of transposases, implying that horizontal gene transfer may be a common occurrence in the deep-sea vent chimney biosphere. In addition, genes for chemotaxis and flagellar assembly were highly enriched in the chimney metagenomes, reflecting the adaptation of the organisms to the highly dynamic conditions present within the chimney walls. Reconstruction of the metabolic pathways revealed that the microbial community in the wall of chimney 4143-1 was mainly fueled by sulfur oxidation, putatively coupled to nitrate reduction to perform inorganic carbon fixation through the Calvin-Benson-Bassham cycle. On the basis of the genomic organization of the key genes of the carbon fixation and sulfur oxidation pathways contained in the large genomic fragments, both obligate and facultative autotrophs appear to be present and contribute to biomass production.

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Autotrophic ammonia oxidation in a deep-sea hydrothermal plume

Cited by 84 publications

References 86 publications

Genome-enabled transcriptomics reveals archaeal populations that drive nitrification in a deep-sea hydrothermal plume

Genome-enabled transcriptomics reveals archaeal populations that drive nitrification in a deep-sea hydrothermal plume

Life without light: microbial diversity and evidence of sulfur- and ammonium-based chemolithotrophy in Movile Cave

Comparative metagenomics of microbial communities inhabiting deep-sea hydrothermal vent chimneys with contrasting chemistries

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