Denitrification in foraminifera has ancient origins and is complemented by associated bacteria

Benthic foraminifera are unicellular eukaryotes that inhabit sediments of aquatic environments. Several foraminifera of the order Rotaliida are known to store and use nitrate for denitrification, a unique energy metabolism among eukaryotes. The rotaliid Globobulimina spp. has been shown to encode an incomplete denitrification pathway of bacterial origins. However, the prevalence of denitrification genes in foraminifera remains unknown and the missing denitrification pathway components are elusive. Analysing transcriptomes and metagenomes of ten foraminifera species from the Peruvian oxygen minimum zone, we show that denitrification genes are highly conserved in foraminifera. We infer of the last common ancestor of denitrifying foraminifera, which enables us to predict further denitrifying species. Additionally, an examination of the foraminifera microbiota reveals evidence for a stable interaction with Desulfobacteracea, which harbour genes that complement the foraminifera denitrification pathway. Our results provide evidence that foraminiferal denitrification is complemented by the foraminifera microbiome. The interaction of Foraminifera with their resident bacteria is at the basis of foraminifera adaptation to anaerobic environments that manifested in ecological success within oxygen depleted habitats.

Substantial oxygen consumption by aerobic nitrite oxidation in oceanic oxygen minimum zones

Oceanic oxygen minimum zones (OMZs) are globally significant sites of biogeochemical cycling where microorganisms deplete dissolved oxygen (DO) to concentrations <20 µM. Amid intense competition for DO in these metabolically challenging environments, aerobic nitrite oxidation may consume significant amounts of DO and help maintain low DO concentrations, but this remains unquantified. Using parallel measurements of oxygen consumption rates and 15N-nitrite oxidation rates applied to both water column profiles and oxygen manipulation experiments, we show that the contribution of nitrite oxidation to overall DO consumption systematically increases as DO declines below 2 µM. Nitrite oxidation can account for all DO consumption only under DO concentrations <393 nM found in and below the secondary chlorophyll maximum. These patterns are consistent across sampling stations and experiments, reflecting coupling between nitrate reduction and nitrite-oxidizing Nitrospina with high oxygen affinity (based on isotopic and omic data). Collectively our results demonstrate that nitrite oxidation plays a pivotal role in the maintenance and biogeochemical dynamics of OMZs.

The Diversity and Nitrogen Metabolism of Culturable Nitrate-Utilizing Bacteria Within the Oxygen Minimum Zone of the Changjiang (Yangtze River) Estuary

The nitrogen cycle is an indispensable part of the biogeochemical cycle, and the reactions that occur in the ocean oxygen minimum zone (OMZ) mediate much of the loss of nitrogen from oceans worldwide. Here, nitrate-utilizing bacteria were isolated from the water column at 17 stations within the OMZ of the Changjiang (Yangtze River) Estuary using selective media and a culture-dependent method. The microbial diversity, nitrogen metabolism and nitrate reduction test of culturable heterotrophic bacteria were examined. A total of 164 isolates were obtained; they were mostly affiliated with Proteobacteria (81.1%), Actinobacteria (5.5%), Bacteroidetes (12.3%), and Firmicutes (0.6%). Pseudomonas aeruginosa, Sphingobium naphthae, and Zunongwangia profunda were found at most stations. Among 24 tested representative strains, 8 were positive for nitrate reduction; they belonged to genera Aurantimonas, Halomonas, Marinobacter, Pseudomonas, Thalassospira, and Vibrio. Pseudomonas aeruginosa contained the genes (napAB, norBC, nirS, and nosZ) for complete denitrification and may be responsible for mediating denitrification. 66% representative isolates (16/24) contained genes for reducing nitrate to nitrite (nasA, napAB, or narGHI) and 79% representative isolates (19/24) possessed genes for converting nitrite to ammonia (nirA or nirBD), suggesting that nitrate and nitrite could act as electron acceptors to generate ammonium, subsequently being utilized as a reduced nitrogen source. This study improves our understanding of the microbial diversity within the OMZ of Changjiang Estuary and may facilitate the cultivation and exploitation of bacteria involved in the nitrogen cycle.

Centennial to millennial variability of greenhouse climate across the mid-Cenomanian event

Centennial- to millennial-scale climate variations are often attributed to solar forcing or internal climate system variability, but recognition of such variations in the deep-time paleoclimate record is extremely rare. We present an exceptionally well-preserved, millimeter-scale laminated marlstone from a succession of precession-driven limestone-marlstone couplets deposited in the Western Interior Seaway (North America) immediately preceding and during the Cretaceous mid-Cenomanian event (ca. 96.5 Ma). Sedimentological, geochemical, and micropaleontological data indicate that individual pairs of light-dark laminae record alternations in the extent of water-column mixing and oxygenation. Principal component analysis of X-ray fluorescence element counts and a grayscale scan of a continuous thin section through the marlstone reveal variations with 80–100 yr, 200–230 yr, 350–500 yr, ~1650 yr, and 4843 yr periodicities. A substantial fraction of the data indicates an anoxic bottom water variation with a pronounced 10,784 yr cycle. The centennial to millennial variations are reminiscent of those found in Holocene total solar irradiance variability, and the 10,784 yr anoxia cycle may be a manifestation of semi-precession-influenced Tethyan oxygen minimum zone waters entering the seaway.

Viral community analysis in a marine oxygen minimum zone indicates increased potential for viral manipulation of microbial physiological state

Microbial communities in oxygen minimum zones (OMZs) are known to have significant impacts on global biogeochemical cycles, but viral influence on microbial processes in these regions are much less studied. Here we provide baseline ecological patterns using microscopy and viral metagenomics from the Eastern Tropical North Pacific (ETNP) OMZ region that enhance our understanding of viruses in these climate-critical systems. While extracellular viral abundance decreased below the oxycline, viral diversity and lytic infection frequency remained high within the OMZ, demonstrating that viral influences on microbial communities were still substantial without the detectable presence of oxygen. Viral community composition was strongly related to oxygen concentration, with viral populations in low-oxygen portions of the water column being distinct from their surface layer counterparts. However, this divergence was not accompanied by the expected differences in viral-encoded auxiliary metabolic genes (AMGs) relating to nitrogen and sulfur metabolisms that are known to be performed by microbial communities in these low-oxygen and anoxic regions. Instead, several abundant AMGs were identified in the oxycline and OMZ that may modulate host responses to low-oxygen stress. We hypothesize that this is due to selection for viral-encoded genes that influence host survivability rather than modulating host metabolic reactions within the ETNP OMZ. Together, this study shows that viruses are not only diverse throughout the water column in the ETNP, including the OMZ, but their infection of microorganisms has the potential to alter host physiological state within these biogeochemically important regions of the ocean.

Evidences and drivers of ocean deoxygenation off Peru over recent past decades

Deoxygenation is a major threat to the coastal ocean health as it impacts marine life and key biogeochemical cycles. Understanding its drivers is crucial in the thriving and highly exploited Peru upwelling system, where naturally low-oxygenated subsurface waters form the so-called oxygen minimum zone (OMZ), and a slight vertical shift in its upper limit may have a huge impact. Here we investigate the long-term deoxygenation trends in the upper part of the nearshore OMZ off Peru over the period 1970–2008. We use a unique set of dissolved oxygen in situ observations and several high-resolution regional dynamical-biogeochemical coupled model simulations. Both observation and model present a nearshore deoxygenation above 150 m depth, with a maximum trend of – 10 µmol kg−1 decade1, and a shoaling of the oxycline depth (− 6.4 m decade−1). Model sensitivity analysis shows that the modeled oxycline depth presents a non-significant (+ 0.9 m decade−1) trend when remote forcing is suppressed, while a significant oxycline shoaling (− 3 m decade−1) is obtained when the wind variability is suppressed. This indicates that the nearshore deoxygenation can be attributed to the slowdown of the near-equatorial eastward currents, which transport oxygen-rich waters towards the Peruvian shores. The large uncertainties in the estimation of this ventilation flux and the consequences for more recent and future deoxygenation trends are discussed.

Causes of uncertainties in the representation of the Arabian Sea oxygen minimum zone in CMIP5 models

Open-ocean oxygen minimum zones (OMZs) occur in regions with high biological productivity and weak ventilation. They restrict marine habitats and alter biogeochemical cycles. Global models generally show a large model–data misfit with regard to oxygen. Reliable statements about the future development of OMZs and the quantification of their interaction with climate change are currently not possible. One of the most intense OMZs worldwide is located in the Arabian Sea (AS). We give an overview of the main model deficiencies with a detailed comparison of the historical state of 10 climate models from the 5th Coupled Model Intercomparison Project (CMIP5) that present our present-day understanding of physical and biogeochemical processes. Most of the models show a general underestimation of the OMZ volume in the AS compared to observations that is caused by an overly shallow layer of oxygen-poor water in the models. The deviation of oxygen values in the deep AS is the result of oxygen levels that are too high simulated in the Southern Ocean formation regions of Indian Ocean Deep Water in the models compared to observations and uncertainties in the deepwater mass transport from the Southern Ocean northward into the AS. Differences in simulated water mass properties and ventilation rates of Red Sea Water and Persian Gulf Water cause different mixing in the AS and thus influence the intensity of the OMZ. These differences in ventilation rates also point towards variations in the parameterizations of the overflow from the marginal seas among the models. The results of this study are intended to foster future model improvements regarding the OMZ in the AS.