skip to main content

Attention:

The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 11:00 PM ET on Friday, May 17 until 8:00 AM ET on Saturday, May 18 due to maintenance. We apologize for the inconvenience.


Title: Patterns of iron and siderophore distributions across the California Current System
Abstract

Coastal upwelling of nutrients and metals along eastern boundary currents fuels some of the most biologically productive marine ecosystems. Although iron is a main driver of productivity in many of these regions, iron cycling and acquisition by microbes remain poorly constrained, in part due to the unknown composition of organic ligands that keep bioavailable iron in solution. In this study, we investigated organic ligand composition in discrete water samples collected across the highly productive California Coastal upwelling system. Siderophores were observed in distinct nutrient regimes at concentrations ranging from 1 pM to 18 pM. Near the shallow continental shelf, ferrioxamine B was observed in recently upwelled, high chlorophyll surface waters while synechobactins were identified within nepheloid layers at 60–90 m depth. In offshore waters characterized by intermediate chlorophyll, iron, and nitrate concentrations, we found amphibactins and an unknown siderophore with a molecular formula of C33H58O8N5Fe. Highest concentrations were measured in the photic zone, however, amphibactins were also found in waters as deep as 1500 m. The distribution of siderophores provides evidence for microbial iron deficiency across a range of nutrient regimes and indicates siderophore production and acquisition is an important strategy for biological iron uptake in iron limited coastal systems. Polydisperse humic ligands were also detected throughout the water column and were particularly abundant near the benthic boundary. Our results highlight the fine‐scale spatial heterogeneity of metal ligand composition in an upwelling environment and elucidate distinct sources that include biological production and the degradation of organic matter in suboxic waters.

 
more » « less
Award ID(s):
1736280
NSF-PAR ID:
10462462
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Limnology and Oceanography
Volume:
64
Issue:
1
ISSN:
0024-3590
Page Range / eLocation ID:
p. 376-389
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. The growth of diatoms in the Southern Ocean, especially the region surrounding the West Antarctic Peninsula, is frequently constrained by low dissolved iron and other trace metal concentrations. This challenge may be overcome by mutualisms between diatoms and co-occurring associated bacteria, in which diatoms produce organic carbon as a substrate for bacterial growth, and bacteria produce siderophores, metal-binding ligands that can supply diatoms with metals upon uptake as well as other useful secondary compounds for diatom growth like vitamins. To examine the relationships between diatoms and bacteria in the plankton (diatom) size class (> 3 µm), we sampled both bacterial and diatom community composition with accompanying environmental metadata across a naturally occurring concentration gradient of macronutrients, trace metals and siderophores at 21 stations near the West Antarctic Peninsula (WAP). Offshore Drake Passage stations had low dissolved iron (0.33 ± 0.15 nM), while the stations closer to the continental margin had higher dissolved iron (5.05 ± 1.83 nM). A similar geographic pattern was observed for macronutrients and most other trace metals measured, but there was not a clear inshore-offshore gradient in siderophore concentrations. The diatom and bacteria assemblages, determined using 18S and 16S rDNA sequencing respectively, were similar by location sampled, and variance in both assemblages was driven in part by concentrations of soluble reactive phosphorous, dissolved manganese, and dissolved copper, which were all higher near the continent. Some of the most common diatom sequence types observed were Thalassiosira and Fragilariopsis , and bacteria in the plankton size fraction were most commonly Bacteroidetes and Gammaproteobacteria. Network analysis showed positive associations between diatoms and bacteria, indicating possible in situ mutualisms through strategies such as siderophore and vitamin biosynthesis and exchange. This work furthers the understanding of how naturally occurring gradients of metals and nutrients influence diatom-bacteria interactions. Our data suggest that distinct groups of diatoms and associated bacteria are interacting under different trace metal regimes in the WAP, and that diatoms with different bacterial partners may have different modes of biologically supplied trace metals. 
    more » « less
  2. ABSTRACT Cyanobacteria are foundational drivers of global nutrient cycling, with high intracellular iron (Fe) requirements. Fe is found at extremely low concentrations in aquatic systems, however, and the ways in which cyanobacteria take up Fe are largely unknown, especially the initial step in Fe transport across the outer membrane. Here, we identified one TonB protein and four TonB-dependent transporters (TBDTs) of the energy-requiring Fe acquisition system and six porins of the passive diffusion Fe uptake system in the model cyanobacterium Synechocystis sp. strain PCC 6803. The results experimentally demonstrated that TBDTs not only participated in organic ferri-siderophore uptake but also in inorganic free Fe (Fe′) acquisition. 55 Fe uptake rate measurements showed that a TBDT quadruple mutant acquired Fe at a lower rate than the wild type and lost nearly all ability to take up ferri-siderophores, indicating that TBDTs are critical for siderophore uptake. However, the mutant retained the ability to take up Fe′ at 42% of the wild-type Fe′ uptake rate, suggesting additional pathways of Fe′ acquisition besides TBDTs, likely by porins. Mutations in four of the six porin-encoding genes produced a low-Fe-sensitive phenotype, while a mutation in all six genes was lethal to cell survival. These diverse outer membrane Fe uptake pathways reflect cyanobacterial evolution and adaptation under a range of Fe regimes across aquatic systems. IMPORTANCE Cyanobacteria are globally important primary producers and contribute about 25% of global CO 2 fixation. Low Fe bioavailability in surface waters is thought to limit the primary productivity in as much as 40% of the global ocean. The Fe acquisition strategies that cyanobacteria have evolved to overcome Fe deficiency remain poorly characterized. We experimentally characterized the key players and the cooperative work mode of two Fe uptake pathways, including an active uptake pathway and a passive diffusion pathway in the model cyanobacterium Synechocystis sp. PCC 6803. Our finding proved that cyanobacteria use ferri-siderophore transporters to take up Fe′, and they shed light on the adaptive mechanisms of cyanobacteria to cope with widespread Fe deficiency across aquatic environments. 
    more » « less
  3. Abstract. The Indian Ocean presents two distinct climate regimes. The north Indian Ocean is dominated by the monsoons, whereas the seasonal reversal is less pronounced in the south. The prevailing wind pattern produces upwelling along different parts of the coast in both hemispheres during different times of the year. Additionally, dynamical processes and eddies either cause or enhance upwelling. This paper reviews the phenomena of upwelling along the coast of the Indian Ocean extending from the tip of South Africa to the southern tip of the west coast of Australia. Observed features, underlying mechanisms, and the impact of upwelling on the ecosystem are presented. In the Agulhas Current region, cyclonic eddies associated with Natal pulses drive slope upwelling and enhance chlorophyll concentrations along the continental margin. The Durban break-away eddy spun up by the Agulhas upwells cold nutrient-rich water. Additionally, topographically induced upwelling occurs along the inshore edges of the Agulhas Current. Wind-driven coastal upwelling occurs along the south coast of Africa and augments the dynamical upwelling in the Agulhas Current. Upwelling hotspots along the Mozambique coast are present in the northern and southern sectors of the channel and are ascribed to dynamical effects of ocean circulation in addition to wind forcing. Interaction of mesoscale eddies with the western boundary, dipole eddy pair interactions, and passage of cyclonic eddies cause upwelling. Upwelling along the southern coast of Madagascar is caused by the Ekman wind-driven mechanism and by eddy generation and is inhibited by the Southwest Madagascar Coastal Current. Seasonal upwelling along the East African coast is primarily driven by the northeast monsoon winds and enhanced by topographically induced shelf breaking and shear instability between the East African Coastal Current and the island chains. The Somali coast presents a strong case for the classical Ekman type of upwelling; such upwelling can be inhibited by the arrival of deeper thermocline signals generated in the offshore region by wind stress curl. Upwelling is nearly uniform along the coast of Arabia, caused by the alongshore component of the summer monsoon winds and modulated by the arrival of Rossby waves generated in the offshore region by cyclonic wind stress curl. Along the west coast of India, upwelling is driven by coastally trapped waves together with the alongshore component of the monsoon winds. Along the southern tip of India and Sri Lanka, the strong Ekman transport drives upwelling. Upwelling along the east coast of India is weak and occurs during summer, caused by alongshore winds. In addition, mesoscale eddies lead to upwelling, but the arrival of river water plumes inhibits upwelling along this coast. Southeasterly winds drive upwelling along the coast of Sumatra and Java during summer, with Kelvin wave propagation originating from the equatorial Indian Ocean affecting the magnitude and extent of the upwelling. Both El Niño–Southern Oscillation (ENSO) and Indian Ocean Dipole (IOD) events cause large variability in upwelling here. Along the west coast of Australia, which is characterized by the anomalous Leeuwin Current, southerly winds can cause sporadic upwelling, which is prominent along the southwest, central, and Gascoyne coasts during summer. Open-ocean upwelling in the southern tropical Indian Ocean and within the Sri Lanka Dome is driven primarily by the wind stress curl but is also impacted by Rossby wave propagations. Upwelling is a key driver enhancing biological productivity in all sectors of the coast, as indicated by enhanced sea surface chlorophyll concentrations. Additional knowledge at varying levels has been gained through in situ observations and model simulations. In the Mozambique Channel, upwelling simulates new production and circulation redistributes the production generated by upwelling and mesoscale eddies, leading to observations of higher ecosystem impacts along the edges of eddies. Similarly, along the southern Madagascar coast, biological connectivity is influenced by the transport of phytoplankton from upwelling zones. Along the coast of Kenya, both productivity rates and zooplankton biomass are higher during the upwelling season. Along the Somali coast, accumulation of upwelled nutrients in the northern part of the coast leads to spatial heterogeneity in productivity. In contrast, productivity is more uniform along the coasts of Yemen and Oman. Upwelling along the west coast of India has several biogeochemical implications, including oxygen depletion, denitrification, and high production of CH4 and dimethyl sulfide. Although weak, wind-driven upwelling leads to significant enhancement of phytoplankton in the northwest Bay of Bengal during the summer monsoon. Along the Sumatra and Java coasts, upwelling affects the phytoplankton composition and assemblages. Dissimilarities in copepod assemblages occur during the upwelling periods along the west coast of Australia. Phytoplankton abundance characterizes inshore edges of the slope during upwelling season, and upwelling eddies are associated with krill abundance. The review identifies the northern coast of the Arabian Sea and eastern coasts of the Bay of Bengal as the least observed sectors. Additionally, sustained long-term observations with high temporal and spatial resolutions along with high-resolution modelling efforts are recommended for a deeper understanding of upwelling, its variability, and its impact on the ecosystem. 
    more » « less
  4. Abstract

    Silicate minerals represent an important reservoir of nutrients at Earth's surface and a source of alkalinity that modulates long‐term geochemical cycles. Due to the slow kinetics of primary silicate mineral dissolution and the potential for nutrient immobilization by secondary mineral precipitation, the bioavailability of many silicate‐bound nutrients may be limited by the ability of micro‐organisms to actively scavenge these nutrients via redox alteration and/or organic ligand production. In this study, we use targeted laboratory experiments with olivine and the siderophore deferoxamine B to explore how microbial ligands affect nutrient (Fe) release and the overall rate of mineral dissolution. Our results show that olivine dissolution rates are accelerated in the presence of micromolar concentrations of deferoxamine B. Based on the non‐linear decrease in rates with time and formation of a Fe3+‐ligand complex, we attribute this acceleration in dissolution rates to the removal of an oxidized surface coating that forms during the dissolution of olivine at circum‐neutralpHin the presence of O2and the absence of organic ligands. While increases in dissolution rates are observed with micromolar concentrations of siderophores, it remains unclear whether such conditions could be realized in natural environments due to the strong physiological control on microbial siderophore production. So, to contextualize our experimental results, we also developed a feedback model, which considers how microbial physiology and ligand‐promoted mineral dissolution kinetics interact to control the extent of biotic enhancement of dissolution rates expected for different environments. The model predicts that physiological feedbacks severely limit the extent to which dissolution rates may be enhanced by microbial activity, though the rate of physical transport modulates this limitation.

     
    more » « less
  5. null (Ed.)
    The genus Phaeocystis is distributed globally and has considerable ecological, biogeochemical, and societal impacts. Understanding its distribution, growth and ecological impacts has been limited by lack of extensive observations on appropriate scales. In 2018, we investigated the biological dynamics of the New England continental shelf and encountered a substantial bloom of Phaeocystis pouchetii. Based on satellite imagery during January through April, the bloom extended over broad expanses of the shelf; furthermore, our observations demonstrated that it reached high biomass levels, with maximum chlorophyll concentrations exceeding 16 μg L−1 and particulate organic carbon levels > 95 μmol L−1. Initially, the bloom was largely confined to waters with temperatures <6°C, which in turn were mostly restricted to shallow areas near the coast. As the bloom progressed, it appeared to sink into the bottom boundary layer; however, enough light and nutrients were available for growth. The bloom was highly productive (net community production integrated through the mixed layer from stations within the bloom averaged 1.16 g C m−2 d−1) and reduced nutrient concentrations considerably. Long-term coastal observations suggest that Phaeocystis blooms occur sporadically in spring on Nantucket Shoals and presumably expand onto the continental shelf. Based on the distribution of Phaeocystis during our study, we suggest that it can have a significant impact on the overall productivity and ecology of the New England shelf during the winter/spring transition. 
    more » « less