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

Abstract

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.

Potential virus-mediated nitrogen cycling in oxygen-depleted oceanic waters

“…First, reduced nitrogen assimilation is known in many cyanobacteria, with nearly all lineages of Prochlorococcus encoding nirA . The potentially high mobility of genes involved with nitrogen assimilation may be justified by the relatively high concentration and energetic favorability of nitrite (relative to ammonia and nitrate) in this system [ 126 ]. Here, we have further identified a cyanophage carrying focA and nirA , suggesting that N assimilation is also of value to the viruses infecting the novel cyanobacteria from the anoxic secondary chlorophyll maximum [ 121 – 123 , 126 ].…”

“…The potentially high mobility of genes involved with nitrogen assimilation may be justified by the relatively high concentration and energetic favorability of nitrite (relative to ammonia and nitrate) in this system [126]. Here, we have further identified a cyanophage carrying focA and nirA, suggesting that N assimilation is also of value to the viruses infecting the novel cyanobacteria from the anoxic secondary chlorophyll maximum [121][122][123]126]. Second, this viral manipulation of the denitrification pathway, via NirK, NorB, and/or NOD-like NorB, underlines the relevance of this pathway in anoxic waters.…”

Size-Fractionated Contribution of Microbial Biomass to Suspended Organic Matter in the Eastern Tropical South Pacific Oxygen Minimum Zone

“…Instead, many are comprised of monounsaturated and saturated fatty acids (the most abundant being MGDG-30:1), which are typically more common in cyanobacteria (Harwood, 1998;Wada and Murata, 1998). The same highly abundant molecule (MGDG-30:1) in the free-living fraction clusters toward moderate pCO 2 and NO 2 − and provides evidence for a distinct bacterial source for the same molecule in the photic zone, possibly attributable to high cell counts of Prochlorococcus in subsurface waters (Lavin et al, 2010;Garcia-Robledo et al, 2017;Aldunate et al, 2020).…”

“…Export of surface-derived photoautotrophic membranes may explain this distribution and a negative correlation to chlorophyll concentration. The negative correlation to chlorophyll may also be explained by the contribution of low-light adapted Prochlorococcus in the chemocline and upper OMZ of the ETSP where chlorophyll concentrations drop rapidly (Garcia-Robledo et al, 2017;Aldunate et al, 2020).…”

Anoxic chlorophyll maximum enhances local organic matter remineralization and nitrogen loss in Lake Tanganyika

“…In marine oxygen-deficient zones, the ACM tends to be dominated by the low-light adapted cyanobacteria genera Prochlorococcus and to a lesser extent by Synechococcus 12,18,[20][21][22] . The marine ACM, which can occur at an irradiance of 5 μmol photons m −2 s −1,18 , is considered a prevalent feature of most marine oxygen-deficient zones 12,18,[20][21][22] and can persist year-round within a stable isopycnal layer 15,23 . Oxygenic photosynthesis by cyanobacteria has been shown to generate molecular oxygen (O 2 ) possibly supporting microaerobic nitrification in the ACM 18 .…”