Cryptic oxygen cycling in anoxic marine zones

García‐Robledo, Emilio; Padilla, Cory C.; Aldunate, Montserrat; Stewart, Frank J.; Ulloa, Osvaldo; Paulmier, Aurélien; Grégori, Gérald; Revsbech, Niels Peter

doi:10.1073/pnas.1619844114

Cited by 122 publications

(186 citation statements)

References 40 publications

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“…Previous studies that analyzed SCMs found conditions within the range observed here (Lavin et al ; Garcia‐Robledo et al ; Widner et al , b ). Dissolved oxygen shows saturation conditions at the surface layer, followed by a pronounced oxycline.…”

Section: Discussionsupporting

confidence: 80%

“…The results indicate that Prochlorococcus and Synechococcus ‐like are using

{NO}_{3}^{-}

and

{NO}_{2}^{-}

in the SCM at extremely low rates for their N requirements and that the potential rates for

{NH}_{4}^{+}

and urea are comparable at least to some of the study sites listed in Table . It is also important to point out that this list in Table shows high variability in the uptake rates ( see Garcia‐Robledo et al for measurements for different stations in the SCM) and that our results are within this variability. The uptake rates obtained for the reduced N forms also support the data obtained for the natural abundance values of δ 15 N, where most of the natural abundance data for the picocyanobacteria were consistent with the δ 15 N of

{NH}_{4}^{+}

/urea or a mixture of these sources including

{NO}_{3}^{-}

and

{NO}_{2}^{-}

.…”

Section: Discussionsupporting

confidence: 74%

“…These SCMs have been found specifically in the oxygen‐deficient zones (ODZs), also known as anoxic marine zones (AMZs), that are distinguished from other oxygen minimum zones by the accumulation of nitrite and the complete absence of detectable oxygen using the most sensitive detectors such as the STOX oxygen sensor (detection limits 1–10 nmol L −1 ; Revsbech et al ; Thamdrup et al ; Ulloa et al ). Nevertheless, these Prochlorococcus have recently been shown to drive a cryptic oxygen cycle that possibly fuels aerobic processes such as

{NO}_{2}^{-}

‐oxidation (Garcia‐Robledo et al ).…”

mentioning

confidence: 99%

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Nitrogen assimilation in picocyanobacteria inhabiting the oxygen‐deficient waters of the eastern tropical North and South Pacific

Aldunate

Henríquez‐Castillo

et al. 2019

Limnology & Oceanography

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Prochlorococcus and Synechococcus are the most abundant free‐living photosynthetic microorganisms in the ocean. Uncultivated lineages of these picocyanobacteria also thrive in the dimly illuminated upper part of oxygen‐deficient zones (ODZs), where an important portion of ocean nitrogen (N) loss takes place via denitrification and anaerobic ammonium oxidation. Recent metagenomic studies revealed that ODZ Prochlorococcus have the genetic potential for using different N forms, including nitrate and nitrite, uncommon N sources for Prochlorococcus, but common for Synechococcus. To determine which N sources ODZ picocyanobacteria are actually using in nature, the cellular 15N natural abundance (δ15N) and assimilation rates of different N compounds were determined using cell sorting by flow cytometry and mass spectrometry. The natural δ15N of the ODZ Prochlorococcus varied from −4.0‰ to 13.0‰ (n = 9), with 50% of the values in the range of −2.1–2.6‰. While the highest values suggest nitrate use, most observations indicate the use of nitrite, ammonium, or a mixture of N sources. Meanwhile, incubation experiments revealed potential assimilation rates of ammonium and urea in the same order of magnitude as that expected for total N in several environments including ODZs, whereas rates of nitrite and nitrate assimilation were very low. Our results thus indicate that reduced forms of N and nitrite are the dominant sources for ODZ picocyanobacteria, although nitrate might be important on some occasions. ODZ picocyanobacteria might thus represent potential competitors with anammox bacteria for ammonium and nitrite, with ammonia‐oxidizing archaea for ammonium, and with nitrite‐oxidizing bacteria for nitrite.

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Section: Discussionsupporting

confidence: 80%

“…The results indicate that Prochlorococcus and Synechococcus ‐like are using

{NO}_{3}^{-}

and

{NO}_{2}^{-}

in the SCM at extremely low rates for their N requirements and that the potential rates for

{NH}_{4}^{+}

{NH}_{4}^{+}

/urea or a mixture of these sources including

{NO}_{3}^{-}

and

{NO}_{2}^{-}

.…”

Section: Discussionsupporting

confidence: 74%

{NO}_{2}^{-}

‐oxidation (Garcia‐Robledo et al ).…”

mentioning

confidence: 99%

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Nitrogen assimilation in picocyanobacteria inhabiting the oxygen‐deficient waters of the eastern tropical North and South Pacific

Aldunate

Henríquez‐Castillo

et al. 2019

Limnology & Oceanography

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“…This threshold is 40 g NaCl/L and is the optimum salinity reported for the most halophilic nitrifying strain (Koops, Böttcher, Möller, Pommerening‐Röser, & Stehr, ). Nitrospina bacteria may tolerate wide fluctuations in oxygen concentrations that could vary from anoxia (Garcia‐Robledo et al., ) to well‐oxygenated conditions as reported here. Moreover, Nitrospina bacteria are resilient to solar radiation (Levipan et al., ), which is an important environmental driver in the upper intertidal zone.…”

Section: Discussionmentioning

confidence: 64%

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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“…Finally, subsurface particles production between 34 and 149 m can affect T eff , for instance when associated with a deep or Secondary Chlorophyll Maximum (SCM), which can sometimes be more intense than the primary maximum in OMZ areas 5 (Garcia-Robledo et al, 2017). The fluorometer data at 31 m suggest an intermittent increase in the fluorescence around this depth ( Fig.…”

mentioning

confidence: 97%

Modulation of the vertical particles transfer efficiency in the Oxygen Minimum Zone off Peru

Bretagnon¹,

Paulmier²,

Garçon³

et al. 2018

Preprint

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Abstract. The fate of the Organic Matter (OM) produced by marine life controls the major biogeochemical cycles of the Earth&#8217;s system. The OM produced through photosynthesis is either preserved, exported towards sediments or degraded through remineralisation in the water column. The productive Eastern Boundary Upwelling Systems (EBUSs) associated with Oxygen Minimum Zones (OMZs) should foster OM preservation due to low O2 conditions, but their intense and diverse microbial activity should enhance OM degradation. To investigate this contradiction, sediment traps were deployed near the oxycline and in the OMZ core on an instrumented moored line off Peru, providing high temporal resolution O2 series characterizing two seasonal steady states at the upper trap: suboxic ([O2]&#8201;<&#8201;25&#8201;&#181;mol&#8201;kg&#8722;1) and hypoxic/oxic (15<[O2]&#8201;<&#8201;160&#8201;&#181;mol&#8201;kg&#8722;1) in austral summer and winter/spring, respectively. The OMZ vertical transfer efficiency of Particulate Organic Carbon (POC) between traps (Teff) fits into three main ranges (high, intermediate, low) suggesting that both predominant preservation (high Teff&#8201;>&#8201;50&#8201;%) and remineralisation (intermediate Teff&#8201;20&#8201;<&#8201;50&#8201;% or low Teff&#8201;<&#8201;6&#8201;%) configurations can occur. An efficient OMZ vertical transfer (Teff&#8201;>&#8201;50&#8201;%) has been reported in summer and winter associated with extreme limitation in O2 concentrations or OM quantity for OM degradation. However, higher levels of O2 or OM, or less refractory OM, at the oxycline, even in a co-limitation context, can decrease the OMZ transfer efficiency below 50&#8201;%, especially in summer during intraseasonal wind-driven oxygenation events. In late winter and early spring, high oxygenation conditions together with high fluxes of sinking particles trigger a shutdown of the OMZ transfer (Teff&#8201;<&#8201;6&#8201;%). Transfer efficiency of chemical elements composing the majority of the flux (nitrogen, phosphorus, silica, calcium carbonate) follows the same trend than for carbon, with the lowest transfer late winter and early spring. In terms of particulate isotopes, vertical transfer of &#948;15N suggests a complex behaviour of 15N impoverishment or enrichment according to Teff modulation. This OM fate sensitivity to O2 fluctuations and particles concentration calls for further investigations on OM and O2-driven remineralisation processes and the consideration of intermittent OMZ behaviour on OM in past studies and climate projections.

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Cryptic oxygen cycling in anoxic marine zones

Cited by 122 publications

References 40 publications

Nitrogen assimilation in picocyanobacteria inhabiting the oxygen‐deficient waters of the eastern tropical North and South Pacific

Nitrogen assimilation in picocyanobacteria inhabiting the oxygen‐deficient waters of the eastern tropical North and South Pacific

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

Modulation of the vertical particles transfer efficiency in the Oxygen Minimum Zone off Peru

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