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Global analysis of ocean phytoplankton nutrient limitation reveals high prevalence of co-limitation - PubMed

  • ️Sun Jan 01 2023

Global analysis of ocean phytoplankton nutrient limitation reveals high prevalence of co-limitation

Thomas J Browning et al. Nat Commun. 2023.

Abstract

Nutrient availability limits phytoplankton growth throughout much of the global ocean. Here we synthesize available experimental data to identify three dominant nutrient limitation regimes: nitrogen is limiting in the stratified subtropical gyres and in the summertime Arctic Ocean, iron is most commonly limiting in upwelling regions, and both nutrients are frequently co-limiting in regions in between the nitrogen and iron limited systems. Manganese can be co-limiting with iron in parts of the Southern Ocean, whilst phosphate and cobalt can be co-/serially limiting in some settings. Overall, an analysis of experimental responses showed that phytoplankton net growth can be significantly enhanced through increasing the number of different nutrients supplied, regardless of latitude, temperature, or trophic status, implying surface seawaters are often approaching nutrient co-limitation. Assessments of nutrient deficiency based on seawater nutrient concentrations and nutrient stress diagnosed via molecular biomarkers showed good agreement with experimentally-assessed nutrient limitation, validating conceptual and theoretical links between nutrient stoichiometry and microbial ecophysiology.

© 2023. Springer Nature Limited.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Global synthesis of nutrient limitation.

a Experimental locations presented on a global map as coloured symbols. b Example experiment. Legend next to example experiment indicates the identities of (co-)limiting nutrient(s) in (a) The central symbol colour(s) on the map indicate the primary limiting nutrient (i.e., adding this nutrient alone stimulated chlorophyll-a accumulation). Outer symbol colours (i.e., colours of the annulus) indicate serial limiting nutrient(s) (i.e., adding this nutrient in addition to the primary limiting nutrient(s) stimulated further growth than supplying the primary limiting nutrient(s) alone). Split colours for inner or outer symbol indicate nutrients that were co-limiting. Sequential levels of serial limitation are indicated by multiple layers of annuli, referencing to secondary limitation (inner annulus) and tertiary limitation (outer annulus). Co-limitation can either be at the primary (split central circle) or serial (split annulus) level. Mesoscale Fe enrichment experiments are shown as crosses. Background colours on map in (a) indicate annual average surface nitrate concentrations. Regions of elevated soluble aerosol Fe deposition predicted by a model are highlighted. Bars in (b) represent the mean chlorophyll-a response to nutrient combinations after 48 h (n = 3 biologically independent samples), dots represent the responses of individual treatments, and the error bars indicate the range. Source data are provided in Supplementary Data 1.

Fig. 2
Fig. 2. Nutrients added within experimental nutrient additions.

Experiments where: (a) a given nutrient was supplied alone; (b) a given nutrient was supplied in any combination. c Maximum number of added nutrients in a given experiment. d Experiments where nutrients were added in full factorial combinations for 2 or 3 nutrients. Experimental and/or individual treatment numbers are indicated in brackets. Source data are provided in Supplementary Data 1.

Fig. 3
Fig. 3. Impact of multiple nutrient addition on estimated net phytoplankton growth.

a, b Without temperature normalization. c, d With temperature-based maximum growth rate normalization (see Methods Eq. 2 and Fig. 4b). Different letters below clusters in (a, c) indicate significantly different means (one-way ANOVA p < 0.05, followed by Tukey Honest Significant Difference test). In (b, d) density refers to the kernel density estimate. Source data are provided in Supplementary Data 1.

Fig. 4
Fig. 4. Relationship of net chlorophyll-a growth rates following experimental nutrient addition with latitude, temperature and trophic status.

a–c Without temperature normalization. The dashed line in (b) is the estimated maxima l growth rate based on an empirical relationship (Eq. 2), which appears to define the upper envelope of responses reasonably well. d–f With temperature-based maximum growth rate normalization (see Methods). Symbol colours indicate numbers of added nutrients within individual experimental treatments. Source data are provided in Supplementary Data 1.

Fig. 5
Fig. 5. Comparison of nutrient limitation and deficiency.

a Experimentally-determined nutrient limitation (see Fig. 1). b Prediction of most deficient nutrient at experimental sites based on seawater nutrient concentrations at the time of experimental water collection, combined with an assumed-average phytoplankton elemental stoichiometry (16 N: 1 P: 7.5 × 10−3 Fe: 2.8 × 10−3 Mn: 8 × 10−4 Zn :1.9 × 10−4 Co; ref. see Methods). c As for (b) but for a fuller range of nutrient elements from the GEOTRACES IDP2017 (V2). Colours correspond to added nutrients as indicated in the legend. Seawater concentrations of vitamin B12 and silicic acid were not included in calculations as they were frequently not reported (vitamin B12) and/or are required by only a few phytoplankton groups (silicic acid). Source data are provided in Supplementary Data 1 and via the publicly accessible GEOTRACES IDP2017 (V2).

Fig. 6
Fig. 6. Relationship of experimentally derived phytoplankton responses to nutrient supply with environmental dissolved nutrient concentration ratios.

a, c Net growth rates derived from changes in chlorophyll-a following N supply were higher at low N:Fe ratios and lower at high N:Fe ratios, with the reverse trend observed for growth rates resulting from Fe supply. Note that N:Fe is in units of mol: mmol. b, d N supply almost always led to higher net chlorophyll-a growth rates than P supply throughout the range of encountered dissolved N:P ratios. Vertical dashed lines represent assumed-average phytoplankton N:Fe (2.13 mol:mmol) and N:P (16 mol:mol) stoichiometry. Blue, red and black symbols indicate N, Fe, and P addition respectively. Split circles indicate the addition of combined N+Fe (blue-red) or N + P (blue-black). Source data are provided in Supplementary Data 1.

Fig. 7
Fig. 7. Experimentally derived nutrient limitation patterns on a background of estimated nitrate upwelling.

Upwelled nitrate was calculated by multiplying the concentration of nitrate immediately below the mixed layer by wind-stress derived Ekman upwelling velocity. Regions of elevated soluble aerosol Fe deposition are highlighted. See Fig. 1 for symbol definitions. Source data are provided in Supplementary Data 1.

Fig. 8
Fig. 8. Distribution of Prochlorococcus nutrient stress as suggested by molecular biomarkers.

Split symbols indicate co-stress by two nutrients. Data points are from the tropical Pacific study of ref. . (highlighted with triangles) and ref. . (all remaining data). Nutrient stressors in ref. . were defined here as (i) the presence of P-II indicating N stress, (ii) the presence of idiA as indicating Fe stress, (iii) the presence of both as indicating N-Fe co-stress. For ref. , all data come from their principal component analysis of nutrient stress genes. Background shading indicates climatological surface nitrate and aerosol Fe deposition (see Fig. 1).

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