skip to main content


Title: Adaptive responses of marine diatoms to zinc scarcity and ecological implications
Abstract

Scarce dissolved surface ocean concentrations of the essential algal micronutrient zinc suggest that Zn may influence the growth of phytoplankton such as diatoms, which are major contributors to marine primary productivity. However, the specific mechanisms by which diatoms acclimate to Zn deficiency are poorly understood. Using global proteomic analysis, we identified two proteins (ZCRP-A/B, Zn/Co Responsive Protein A/B) among four diatom species that became abundant under Zn/Co limitation. Characterization using reverse genetic techniques and homology data suggests putative Zn/Co chaperone and membrane-bound transport complex component roles for ZCRP-A (a COG0523 domain protein) and ZCRP-B, respectively. Metaproteomic detection of ZCRPs along a Pacific Ocean transect revealed increased abundances at the surface (<200 m) where dZn and dCo were scarcest, implying Zn nutritional stress in marine algae is more prevalent than previously recognized. These results demonstrate multiple adaptive responses to Zn scarcity in marine diatoms that are deployed in low Zn regions of the Pacific Ocean.

 
more » « less
Award ID(s):
1850719 2048774 2123055 1924554
NSF-PAR ID:
10381744
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ;
Publisher / Repository:
Nature Publishing Group
Date Published:
Journal Name:
Nature Communications
Volume:
13
Issue:
1
ISSN:
2041-1723
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    The importance of zinc (Zn) as a nutrient and its ability to be substituted for by cobalt (Co) have been characterized in model marine diatoms. However, the extent to which this substitution capability is distributed among diatom taxa is unknown. Zn/Co metabolic substitution was assayed in four diatom species as measured by the effect of free ion concentrations of Zn2+and Co2+on specific growth rate. Analysis of growth responses found substitution of these metals can occur within the northwest Atlantic isolateThalassiosira pseudonanaCCMP1335, the northeast Atlantic isolatePhaeodactylum tricornutumCCMP632, and within the northeast Pacific isolatesPseudo‐nitzschia delicatissimaUNC1205 andThalassiosirasp. UNC1203. Metabolic substitution of Co in place of Zn in the Atlantic diatoms supports their growth in media lacking added Zn, but at the cost of reduced growth rates. In contrast, highly efficient Zn/Co substitution that supported growth even in media lacking added Zn was observed in the northeast Pacific diatoms. We also present new data from the northeast Pacific Line P transect that revealed dissolved Co and Zn ratios (dCo : dZn) as high as 3.52 : 1 at surface (0–100 m) depths. We posit that the enhanced ability of the NE Pacific diatoms to grow using Co is an adaptation to these high surface dCo : dZn ratios. Particulate metal data and single‐cell metal quotas also suggest a high Zn demand in diatoms that may be partially compensated for by Co.

     
    more » « less
  2. Abstract

    Transition metal cofactors are crucial for many biological processes. Despite being primarily considered to be toxic, the transition metal cadmium (Cd) was discovered to be a substitute cofactor for zinc (Zn) in photosynthetic carbon fixation pathways of marine diatoms. However, it is not known how conditions in the geosphere impacted Cd availability and its incorporation as an alternative metal cofactor for phytoplankton. We employed mineral chemistry network analysis to investigate which geochemical factors may have influenced the availability of Cd and Zn during the putative time period that the alternative Cd‐based pathway evolved. Our results show that Zn minerals are more chemically diverse than are Cd minerals, but Zn‐ and Cd‐containing minerals have similar network centrality values when specifically considering sulfur (S)‐containing species. Cadmium and Zn sulfides are the most common Cd‐ and Zn‐containing mineral species over the past 500 million years. In particular, the Cd and Zn sulfides, respectively greenockite and sphalerite, were highly abundant during this time period. Furthermore, S‐containing Cd and Zn minerals are commonly co‐located in geologic time, allowing them to be weathered and transported to the ocean in tandem, rather than from separate sources. We suggest that the simultaneous weathering of Cd and Zn sulfides allowed for Cd to be a bioavailable direct substitute for Zn in protein complexes during periods of Zn depletion. The biogeochemical cycles of Zn and Cd exemplify the importance of the coevolution of the geosphere and biosphere in shaping primary production in the modern ocean.

     
    more » « less
  3. Abstract

    Atmospheric deposition represents a major input for micronutrient trace elements (TEs) to the surface ocean and is often quantified indirectly through measurements of aerosol TE concentrations. Sea spray aerosol (SSA) dominates aerosol mass concentration over much of the global ocean, but few studies have assessed its contribution to aerosol TE loading, which could result in overestimates of “new” TE inputs. Low‐mineral aerosol concentrations measured during the U.S. GEOTRACES Pacific Meridional Transect (GP15; 152°W, 56°N to 20°S), along with concurrent towfish sampling of surface seawater, provided an opportunity to investigate this aspect of TE biogeochemical cycling. Central Pacific Ocean surface seawater Al, V, Mn, Fe, Co, Ni, Cu, Zn, and Pb concentrations were combined with aerosol Na data to calculate a “recycled” SSA contribution to aerosol TE loading. Only vanadium was calculated to have a SSA contribution averaging >1% along the transect (mean of 1.5%). We derive scaling factors from previous studies on TE enrichments in the sea surface microlayer and in freshly produced SSA to assess the broader potential for SSA contributions to aerosol TE loading. Maximum applied scaling factors suggest that SSA could contribute significantly to the aerosol loading of some elements (notably V, Cu, and Pb), while for others (e.g., Fe and Al), SSA contributions largely remained <1%. Our study highlights that a lack of focused measurements of TEs in SSA limits our ability to quantify this component of marine aerosol loading and the associated potential for overestimating new TE inputs from atmospheric deposition.

     
    more » « less
  4. Abstract

    The fate of diatoms in future acidified oceans could have dramatic implications on marine ecosystems, because they account for ~40% of marine primary production. Here, we quantify resilience ofThalassiosira pseudonanain mid-20th century (300 ppm CO2) and future (1000 ppm CO2) conditions that cause ocean acidification, using a stress test that probes its ability to recover from incrementally higher amount of low-dose ultraviolet A (UVA) and B (UVB) radiation and re-initiate growth in day–night cycles, limited by nitrogen. While all cultures eventually collapse, those growing at 300 ppm CO2succumb sooner. The underlying mechanism for collapse appears to be a system failure resulting from “loss of relational resilience,” that is, inability to adopt physiological states matched to N-availability and phase of the diurnal cycle. Importantly, under elevated CO2conditions diatoms sustain relational resilience over a longer timeframe, demonstrating increased resilience to future acidified ocean conditions. This stress test framework can be extended to evaluate and predict how various climate change associated stressors may impact microbial community resilience.

     
    more » « less
  5. Abstract

    This study traces dissolved organic matter (DOM) in different water masses of the Arctic Ocean and its effect on the distributions of trace elements (TEs; Fe, Cu, Mn, Ni, Zn, Cd) using fluorescent properties of DOM and the terrigenous biomarker lignin. The Nansen, Amundsen, and Makarov Basins were characterized by the influence of Atlantic water and the fluvial discharge of the Siberian Rivers with high concentrations of terrigenous DOM (tDOM). The Canada Basin and the Chukchi Sea were characterized by Pacific water, modified through contact with productive shelf sediments with elevated levels of marine DOM. Within the surface layer of the Beaufort Gyre, meteoric water (river water and precipitation) was characterized by low concentrations of lignin and tDOM fluorescence proxies as DOM is removed during freezing. High‐resolution in situ fluorescence profiles revealed that DOM distribution closely followed isopycnals, indicating the strong influence of sea‐ice formation and melt, which was also reflected in strong correlations between DOM fluorescence and brine contributions. The relationship of DOM and hydrography to TEs showed that terrigenous and marine DOM were likely carriers of dissolved Fe, Ni, Cu from the Eurasian shelves into the central Arctic Ocean. Chukchi shelf sediments were important sources of dCd, dZn, and dNi, as well as marine ligands that bind and carry these TEs offshore within the upper halocline in the Canada Basin. Our data suggest that tDOM components represent stronger ligands relative to marine DOM components, potentially facilitating the long‐range transport of TE to the North Atlantic.

     
    more » « less