Major role of nitrite-oxidizing bacteria in dark ocean carbon fixation

Pachiadaki, Maria; Sintes, Eva; Bergauer, Kristin; Brown, Julia; Record, Nicholas R.; Swan, Brandon K.; Mathyer, Mary Elizabeth; Hallam, Steven J.; López‐García, Purificación; Takaki, Yoshihiro; Nunoura, Takuro; Woyke, Tanja; Herndl, Gerhard J.; Stepanauskas, Ramunas

doi:10.1126/science.aan8260

Cited by 223 publications

(232 citation statements)

References 66 publications

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“…However, again it is unclear where the source of sulphide would come from at our study sites since POC fluxes here are low (Lutz et al ; Amon et al ). Nitrite oxidation (Pachiadaki et al ), hydrogen oxidation resulting from the radiolysis of water (D'Hondt et al ), and oxidation of reduced iron or manganese particles that have been deposited from nearby hydrothermal vent sites (Resing et al ; Tully and Heidelberg ) could offer alternative energy sources for at least some of the inorganic C fixation. Alternatively, it could be the result of heterotrophic bacteria using anaplerotic C‐fixation mechanisms.…”

Section: Discussionmentioning

confidence: 99%

Key role of bacteria in the short‐term cycling of carbon at the abyssal seafloor in a low particulate organic carbon flux region of the eastern Pacific Ocean

Sweetman

Smith

Shulse

et al. 2018

Limnology & Oceanography

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The cycling of carbon (C) by benthic organisms is a key ecosystem function in the deep sea. Pulse‐chase experiments are designed to quantify this process, yet few studies have been carried out using abyssal (3500–6000 m) sediments and only a handful of studies have been undertaken in situ. We undertook eight in situ pulse‐chase experiments in three abyssal strata (4050–4200 m water depth) separated by tens to hundreds of kilometers in the eastern Clarion‐Clipperton Fracture Zone (CCFZ). These experiments demonstrated that benthic bacteria dominated the consumption of phytodetritus over short (~ 1.5 d) time scales, with metazoan macrofauna playing a minor role. These results contrast with the only other comparable in situ abyssal study, where macrofauna dominated phytodetritus assimilation over short (2.5 d) time scales in the eutrophic NE Atlantic. We also demonstrated that benthic bacteria were capable of converting dissolved inorganic C into biomass and showed that this process can occur at rates that are as high as the bacterial assimilation of algal‐derived organic C. This demonstrates the potential importance of inorganic C uptake to abyssal ecosystems in this region. It also alludes to the possibility that some of the C incorporation by bacteria in our algal‐addition studies may have resulted from the incorporation of labeled dissolved inorganic carbon initially respired by other unstudied organisms. Our findings reveal the key importance of benthic bacteria in the short‐term cycling of C in abyssal habitats in the eastern CCFZ and provide important information on benthic ecosystem functioning in an area targeted for commercial‐scale, deep‐sea mining activities.

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Section: Discussionmentioning

confidence: 99%

Key role of bacteria in the short‐term cycling of carbon at the abyssal seafloor in a low particulate organic carbon flux region of the eastern Pacific Ocean

Sweetman

Smith

Shulse

et al. 2018

Limnology & Oceanography

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“…Nutritional deprivation in deep-sea environments may limit the productivity of an ecosystem. In addition to recalcitrant materials recycled by deep-sea bacteria, organic carbon produced by CO 2 fixation can be supplied by ammonia-oxidizing and nitrite-oxidizing prokaryotes (Pachiadaki et al, 2017). Ammonia-oxidizing archaea (AOA) are ubiquitous in oxic environments on Earth ranging from shallow waters to deep-sea zones and soils (Karner et al, 2001;Leininger et al, 2006;Park et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Genomics insights into ecotype formation of ammonia‐oxidizing archaea in the deep ocean

Wang

Huang

Cui

et al. 2019

Environmental Microbiology

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Summary Various lineages of ammonia‐oxidizing archaea (AOA) are present in deep waters, but the mechanisms that determine ecotype formation are obscure. We studied 18 high‐quality genomes of the marine group I AOA lineages (alpha, gamma and delta) from the Mariana and Ogasawara trenches. The genomes of alpha AOA resembled each other, while those of gamma and delta lineages were more divergent and had even undergone insertion of some phage genes. The instability of the gamma and delta AOA genomes could be partially due to the loss of DNA polymerase B (polB) and methyladenine DNA glycosylase (tag) genes responsible for the repair of point mutations. The alpha AOA genomes harbour genes encoding a thrombospondin‐like outer membrane structure that probably serves as a barrier to gene flow. Moreover, the gamma and alpha AOA lineages rely on vitamin B12‐independent MetE and B12‐dependent MetH, respectively, for methionine synthesis. The delta AOA genome contains genes involved in uptake of sugar and peptide perhaps for heterotrophic lifestyle. Our study provides insights into co‐occurrence of cladogenesis and anagenesis in the formation of AOA ecotypes that perform differently in nitrogen and carbon cycling in dark oceans.

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“…Alternatively, urease‐like genes in Nitrospina (Ngugi et al., ) could convert fish‐derived urea into ammonium. This ultimately will lead to favored coupling between Nitrospina and ammonia oxidizers (Pachiadaki et al., ). There is experimental evidence that fish metabolism stimulates the nitrification including the transcriptional activity of Nitrospina (Elizondo‐Patrone, Hernández, Yannicelli, Olsen, & Molina, ).…”

Section: Discussionmentioning

confidence: 99%

“…The NOB guild is a functional group that includes phylogenetically distant bacteria belonging to hitherto seven genera distributed over four phyla including the phylum Nitrospinae (Daims, Lücker, & Wagner, ). Members of this phylum have been detected in the field and are basically related to marine chemolithotrophic nitrification (Pachiadaki et al., ). Nitrospina ‐like bacteria have been detected from the surface down to the deep ocean (DeLong et al., ; Nunoura et al., ; Santoro, Casciotti, & Francis, ; Watson & Waterbury, ) including in oxygen minimum zones (OMZs) (Beman, Shih, & Popp, ; Fuchsman, Kirkpatrick, Brazelton, Murray, & Staley, ; Labrenz, Jost, & Jurgens, ; Zaikova et al., ), oxic/anoxic sediments (Davis, Stakes, Wheat, & Moyer, ; Jorgensen et al., ; Rani, Koh, Rhee, Fujitani, & Park, ), and deep estuarine environments (Colatriano et al., ).…”

Section: Introductionmentioning

confidence: 99%

Nitrospina bacteria in a rocky intertidal habitat (Quintay Bay, central Chile)

2018

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Nitrospina bacteria are among the most important nitrite oxidizers in coastal and open-ocean environments, but the relevance of the genus contrasts with the scarceness of information on their ecophysiology and habitat range. Thus far, Nitrospina bacteria have been the only nitrite oxidizers detected at high abundance in Chilean coastal waters. These levels are often higher than at other latitudes. In this study, the abundance of 16S-rRNA gene transcripts of Nitrospina (hereafter just transcripts) was measured by reverse transcription quantitative PCR in a rocky intertidal gradient and compared with the nearshore counterpart off central Chile (~33°S). Rocky pond transcripts were also compared with the taxonomic composition of the macrobiota and bacterioplankton (by 16S-rRNA gene-based T-RFLP) in the intertidal gradient. Transcripts increased from warmer, saltier, and low-nitrite ponds in the upper intertidal zone (19.5 ± 1.6°C, 39.0 ± 1.0 psu, 0.98 ± 0.17 μmol/L) toward cooler, less salty, and high-nitrite ponds (17.8 ± 2.6°C, 37.7 ± 0.82 psu, 1.23 ± 0.21 μmol/L) from middle and low zones. These varied from ~1,000 up to 62,800 transcripts. This increasing trend in the number of transcripts toward the lower zone was positively associated with the Shannon's diversity index for the macrobiota (r = .81, p < .01). Moreover, an important increase in the average number of transcripts was observed in ponds with a greater number of fish in the upper (7,846 transcripts during 2013) and lower zones (62,800 transcripts during 2015). Altogether, intertidal and nearshore transcripts were significantly correlated with nitrite concentrations (r = .804, p ˂ .01); rocky pond transcripts outnumbered nearshore ones by almost two orders of magnitude. In summary, rocky ponds favored both the presence and activity of Nitrospina bacteria that are tolerant to environmental stress. This in turn was positively influenced by the presence of ammonia- or urea-producing macrobiota.

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Major role of nitrite-oxidizing bacteria in dark ocean carbon fixation

Cited by 223 publications

References 66 publications

Key role of bacteria in the short‐term cycling of carbon at the abyssal seafloor in a low particulate organic carbon flux region of the eastern Pacific Ocean

Key role of bacteria in the short‐term cycling of carbon at the abyssal seafloor in a low particulate organic carbon flux region of the eastern Pacific Ocean

Genomics insights into ecotype formation of ammonia‐oxidizing archaea in the deep ocean

Nitrospina bacteria in a rocky intertidal habitat (Quintay Bay, central Chile)

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