Nutrient limitation suppresses the temperature dependence of phytoplankton metabolic rates

Climate warming has the potential to alter ecosystem function through temperature-dependent changes in individual metabolic rates. The temperature sensitivity of phytoplankton metabolism is especially relevant, since these microorganisms sustain marine food webs and are major drivers of biogeochemical cycling. Phytoplankton metabolic rates increase with temperature when nutrients are abundant, but it is unknown if the same pattern applies under nutrient-limited growth conditions, which prevail over most of the ocean. Here we use continuous cultures of three cosmopolitan and biogeochemically relevant species (Synechococcus sp., Skeletonema costatum and Emiliania huxleyi) to determine the temperature dependence (activation energy, Ea) of metabolism under different degrees of nitrogen (N) limitation. We show that both CO2 fixation and respiration rates increase with N supply but are largely insensitive to temperature. Ea of photosynthesis (0.11 ± 0.06 eV, mean ± SE) and respiration (0.04 ± 0.17 eV) under N-limited growth is significantly smaller than Ea of growth rate under nutrient-replete conditions (0.77 ± 0.06 eV). The reduced temperature dependence of metabolic rates under nutrient limitation can be explained in terms of enzyme kinetics, because both maximum reaction rates and half-saturation constants increase with temperature. Our results suggest that the direct, stimulating effect of rising temperatures upon phytoplankton metabolic rates will be circumscribed to ecosystems with high-nutrient availabilityMinisterio de Economía y Competitividad | Ref. CTM2014-53582-

Coccolithophore calcification is independent of carbonate chemistry in the tropical ocean

Marañón, Emilio ... et al.-- 13 pages, 7 figures, 1 table, supporting information https://dx.doi.org/10.1002/lno.10295Short-term experiments indicate that seawater acidification can cause a decrease in the rate of calcification by coccolithophores, but the relationship between carbonate chemistry and coccolithophore calcification rate in natural assemblages is still unclear. During the Malaspina 2010 circumnavigation, we measured primary production, calcification, coccolithophore abundance, particulate inorganic carbon (PIC) concentration, and the parameters of the carbonate system, along basin-scale transects in the tropical Atlantic, Indian and Pacific oceans. Euphotic layer-integrated calcification and mean cell-specific calcification in the euphotic layer ranged between 2–10 mgC m−2 d−1 and 5–20 pgC cell−1 d−1, respectively. We found a significant relationship between primary production and calcification, such that the calcification to primary production (CP/PP) ratio was relatively invariant among ocean basins, with an overall mean value of 0.05 ± 0.04. Extrapolating this value to the entire ocean would result in a global pelagic calcification rate of 2.4 PtC yr−1. The mean PIC concentration in surface waters was 1.8 ± 1.6 mgC m−3 and its turnover time averaged 20 d. We combined our data of calcification, primary production, and carbonate chemistry from Malaspina 2010 with those obtained during two previous cruises in the northern Arabian Sea. Both the CP/PP ratio and cell-specific calcification were largely constant across a wide range of calcite saturation state (1.5–6.5), [ inline image]/[H+] (0.08–0.24; mol: μmol), and pH (7.6–8.1), which indicates that calcification by natural coccolithophore assemblages was independent of carbonate chemistry. Our results suggest that coccolithophore calcification, at least in tropical regions, may not be decreasing in the currently acidifying oceanFunding for this study was provided by the Spanish Ministry of Science and Innovation through research projects Malaspina 2010 (grant no. CSD2008-00077), PERSEO (CTM2007-28925-E/MAR), MANIFEST (CTM2012-32017) and TERRIFIC (CTM2014-53582-R). Funding for W.M.B. came from the NSF (OCE-0961660; OCE1220068), NASA (NNX11AO72G; NNX11AL93G; NNX14AQ41G; NNX14AQ43A; NNX14AL92G; NNX14AM77G) and NOAA (NA11OAR4310055).Peer Reviewe

Nutrient supply does play a role on the structure of marine picophytoplankton communities

Conference communicationThe Margalef´s mandala (1978) is a simplified bottom-up control model that explains how mixing and nutrient concentration determine the composition of marine phytoplankton communities. Due to the difficulties of measuring turbulence in the field, previous attempts to verify this model have applied different proxies for nutrient supply, and very often used interchangeably the terms mixing and stratification. Moreover, because the mandala was conceived before the discovery of smaller phytoplankton groups (picoplankton <2 µm), it describes only the succession of vegetative phases of microplankton. In order to test the applicability of the classical mandala to picoplankton groups, we used a multidisciplinary approach including specifically designed field observations supported by remote sensing, database analyses, and modeling and laboratory chemostat experiments. Simultaneous estimates of nitrate diffusive fluxes, derived from microturbulence observations, and picoplankton abundance collected in more than 200 stations, spanning widely different hydrographic regimes, showed that the contribution of eukaryotes to picoautotrophic biomass increases with nutrient supply, whereas that of picocyanobacteria shows the opposite trend. These findings were supported by laboratory and modeling chemostat experiments that reproduced the competitive dynamics between picoeukaryote sand picocyanobacteria as a function of changing nutrient supply. Our results indicate that nutrient supply controls the distribution of picoplankton functional groups in the ocean, further supporting the model proposed by Margalef.Spanish Governmen

A global compilation of coccolithophore calcification rates

The biological production of calcium carbonate (CaCO3), a process termed calcification, is a key term in the marine carbon cycle. A major planktonic group responsible for such pelagic CaCO3 production (CP) is the coccolithophores, single-celled haptophytes that inhabit the euphotic zone of the ocean. Satellite-based estimates of areal CP are limited to surface waters and open-ocean areas, with current algorithms utilising the unique optical properties of the cosmopolitan bloom-forming species Emiliania huxleyi, whereas little understanding of deep-water ecology, optical properties or environmental responses by species other than E. huxleyi is currently available to parameterise algorithms or models. To aid future areal estimations and validate future modelling efforts we have constructed a database of 2765 CP measurements, the majority of which were measured using 12 to 24 h incorporation of radioactive carbon (14C) into acid-labile inorganic carbon (CaCO3). We present data collated from over 30 studies covering the period from 1991 to 2015, sampling the Atlantic, Pacific, Indian, Arctic and Southern oceans. Globally, CP in surface waters ( < 20 m) ranged from 0.01 to 8398 µmol C m−3 d−1 (with a geometric mean of 16.1 µmol C m−3 d−1). An integral value for the upper euphotic zone (herein surface to the depth of 1 % surface irradiance) ranged from  < 0.1 to 6 mmol C m−2 d−1 (geometric mean 1.19 mmol C m−2 d−1). The full database is available for download from PANGAEA at https://doi.org/10.1594/PANGAEA.888182

Export and turnover of transparent exopolymer particles into the deep ocean

2nd Meeting of the Iberian Ecological Society (SIBECOL), XXI conference of the Iberian Association of Limnology (AIL) and 21st National Congress of the Portuguese Ecological Society (SPECO), 3-8 July 2022, AveiroAcidic polysaccharides released by phytoplankton and prokaryotic heterotrophs promote the formation of gel-like transparent exopolymer particles (TEPs). TEPs play a key role in the biological carbon pump due to their carbon-rich composition and their ability to coagulate and sink towards the deep ocean. Yet, very little is known about TEP distribution, export, and turnover at a global scale, particularly at deep ocean depths. We provide the first inventory of TEP from the surface up to 4000 m depth in the Atlantic, Indian, and Pacific Oceans and have assessed their contribution to carbon export into the deep ocean. Primary production determines TEP concentration above the deep chlorophyll maximum, and prokaryotic biomass also contributes in deeper waters. In the deep ocean waters, TEP concentrations are lower and mirror the concentrations in the surface, evidencing the importance of TEP sinking both at the export depth (200 m) with a global value of 2.9 Pg C year-1 and at the sequestration depth (1000 m) of 0.9 Pg C year-1 of particulate carbon. However, incubation experiments across ocean basins depicted rapid TEP turnover rates of 71 and 333 days (on average) within the export and sequestration depths, respectively. These findings reveal that the export of carbon by TEP sinking towards deep oceans escapes from long-term paths of the global carbon cycleN

Large carbon export, but short residence times, of transparent exopolymer particles in the global ocean

ASLO Aquatic Sciences Meeting 2023, Resilience and Recovery in Aquatic Systems, 4–9 June 2023, Palma de Mallorca, SpainAcidic polysaccharides released by phytoplankton and prokaryotic heterotrophs promote the formation of gel-like transparent exopolymer particles (TEPs). TEPs can have a relevant contribution to the biological carbon pump due to their carbon-rich composition and their ability to coagulate and sink towards the deep ocean. However, little is known about TEPs distribution, carbon export, and residence times below the export (200 m) and sequestration (1000 m) depths. We provide the first comprehensive inventory of TEP from the ocean surface to a depth of 4000 meters in the tropical and subtropical Atlantic, Indian, and Pacific Oceans, evaluating its contribution to carbon export and sequestration into the deep ocean. Results indicate that TEP concentration is primarily determined by primary production, with higher concentrations located above the deep chlorophyll maxima. In the deep ocean, TEP concentrations are lower yet mirror the concentrations in the surface, demonstrating the significance of TEP sinking below both the export compartment (2.8 Pg C yr-1; 27% of total POC flux at 200 m) and the sequestration compartment (0.8 Pg C yr-1; 36% of total POC flux at 1000 m). In situ incubation experiments conducted across ocean basins indicate short TEP residence times, averaging 27 and 333 days in the export and sequestration compartments, respectively. These findings reveal that the export and subsequent sequestration of carbon by TEP sinking into the deep ocean diverts it from the long times observed for the dissolved carbon fraction (i.e. centuries) in the global carbon cycleN

Resource Supply Overrides Temperature as a Controlling Factor of Marine Phytoplankton Growth

The universal temperature dependence of metabolic rates has been used to predict how ocean biology will respond to ocean warming. Determining the temperature sensitivity of phytoplankton metabolism and growth is of special importance because this group of organisms is responsible for nearly half of global primary production, sustains most marine food webs, and contributes to regulate the exchange of CO2 between the ocean and the atmosphere. Phytoplankton growth rates increase with temperature under optimal growth conditions in the laboratory, but it is unclear whether the same degree of temperature dependence exists in nature, where resources are often limiting. Here we use concurrent measurements of phytoplankton biomass and carbon fixation rates in polar, temperate and tropical regions to determine the role of temperature and resource supply in controlling the large-scale variability of in situ metabolic rates. We identify a biogeographic pattern in phytoplankton metabolic rates, which increase from the oligotrophic subtropical gyres to temperate regions and then coastal waters. Variability in phytoplankton growth is driven by changes in resource supply and appears to be independent of seawater temperature. The lack of temperature sensitivity of realized phytoplankton growth is consistent with the limited applicability of Arrhenius enzymatic kinetics when substrate concentrations are low. Our results suggest that, due to widespread resource limitation in the ocean, the direct effect of sea surface warming upon phytoplankton growth and productivity may be smaller than anticipated

Nutrient limitation suppresses the temperature dependence of phytoplankton metabolic rates

10 pages, 5 figures, supplementary material https://doi.org/10.1038/s41396-018-0105-1Climate warming has the potential to alter ecosystem function through temperature-dependent changes in individual metabolic rates. The temperature sensitivity of phytoplankton metabolism is especially relevant, since these microorganisms sustain marine food webs and are major drivers of biogeochemical cycling. Phytoplankton metabolic rates increase with temperature when nutrients are abundant, but it is unknown if the same pattern applies under nutrient-limited growth conditions, which prevail over most of the ocean. Here we use continuous cultures of three cosmopolitan and biogeochemically relevant species (Synechococcus sp., Skeletonema costatum and Emiliania huxleyi) to determine the temperature dependence (activation energy, Ea) of metabolism under different degrees of nitrogen (N) limitation. We show that both CO2 fixation and respiration rates increase with N supply but are largely insensitive to temperature. Ea of photosynthesis (0.11 ± 0.06 eV, mean ± SE) and respiration (0.04 ± 0.17 eV) under N-limited growth is significantly smaller than Ea of growth rate under nutrient-replete conditions (0.77 ± 0.06 eV). The reduced temperature dependence of metabolic rates under nutrient limitation can be explained in terms of enzyme kinetics, because both maximum reaction rates and half-saturation constants increase with temperature. Our results suggest that the direct, stimulating effect of rising temperatures upon phytoplankton metabolic rates will be circumscribed to ecosystems with high-nutrient availabilityP.C. was supported by a Ramón y Cajal contract from the Spanish Ministry of Economy and Competitiveness (MINECO). This research was funded by MINECO through grant CTM2014-53582-R to E.M.Peer reviewe

SPEAD 1.0 -- A model for simulating plankton evolution with adaptive dynamics in a two trait continuous fitness landscape applied to the Sargasso Sea

Diversity plays a key role in ecosystem adaptive capacities. However, modeling phytoplankton trait diversity remains challenging due to the strength of the competitive exclusion of sub-optimal phenotypes. A recent approach to sustain diversity, called "trait diffusion", consists in allowing evolution to occur at contemporary timescales. In this study, we present a model for Simulating Plankton Evolution with Adaptive Dynamics (SPEAD), where phenotypes characterized by two traits, nitrogen half-saturation constant and optimal temperature, can mutate at each generation. SPEAD does not resolve all phenotypes, computing instead six aggregate properties: biomass, mean traits, trait variances and inter-trait covariance. The adaptive dynamics are driven by vertical and seasonal variations in water temperature, irradiance, vertical mixing, and nutrient concentration. The bulk properties are validated by observations from station BATS in the Sargasso Sea. We find only minor discrepancies between SPEAD and a similar model that represents the full phenotype distribution, but SPEAD has a lower computational cost by two orders of magnitude. Moderate mutation rates are shown to sustain trait diversity at decadal timescales and to soften the almost total inter-trait covariance induced by the environment alone, without reducing the annual primary production or promoting permanently maladapted phenotypes, as occurs with high mutation rates. The response to environmental changes is faster than in single-trait models. Future axes of improvement include increasing the number of traits, beginning with optimal irradiance, refining the description of the phytoplankton community by resolving several functional groups, and coupling SPEAD with a general circulation mode