Comparing Prochlorococcus temperature niches in the lab and across ocean basins

Abstract

Niche theory suggests that the realized niche occupied by an organism in the field is a subset of the fundamental niche space of the organism, absent additional biotic and abiotic factors. Though often assumed, this discrepancy is rarely tested for specific organisms, and could act as a source of error in model predictions of biogeographical shifts resulting from temperature change which assume niche theory constraints. Here, we quantify the difference between fundamental and realized temperature niches for four dominant ecotypes of Prochlorococcus, including eMED4, eMIT9312, eMIT9313, and eNATL2A, and ask whether the realized temperature niches of each ecotype vary across ocean basins. The realized niches for the four ecotypes are, on average, 3.84 C AE 1.18 C colder (mean AE SD across all ocean basins and ecotypes) and 2.15 C AE 1.89 C wider than the labmeasured fundamental niches. When divided into four ocean regions-North Atlantic, South Atlantic, North Pacific, and South Pacific-we find that the realized temperature niche optimum for a given ecotype compared to the fundamental temperature niche optimum differs across regions by as much as 7.93 C, while the niche width can differ by up to 9.48 C. Colder and wider realized niches may be a result of the metabolic risk associated with living in variable environments when the mean temperature is too close to the optimal temperature for growth or due to physical processes such as dispersal. The strong differences in temperature niches across ocean basins suggest that unresolved genetic diversity within ecotypes, local adaptation, and variable interactive ecological and environmental factors are likely to be important in shaping Prochlorococcus realized temperature niches.

Effects of dispersal and temperature variability on phytoplankton realized temperature niches

“…The species in our model did, however, have realized niche optima that were, on average, slightly colder than the fundamental temperature niche optimums (𝛿 T opt < 0; Figure 9b). Previous studies (Kingsolver et al, 2013;Smith et al, 2021) have observed this pattern across a range of organisms. Fundamental temperature niches are typically, and in this model, assumed to have a left-or negativelyskewed curve where growth above the optimum temperature decreases rapidly compared to growth below the optimum, as measured from laboratory experiments where growth is calculated from incubations at constant temperatures (Anderson et al, 2021;Norberg, 2004;Thomas et al, 2012).…”

“…Phytoplankton growth for each species in each box (here we drop the j subscript) is a function of temperature (Thomas et al., 2012):$$$$ {\mu}_i(T)=a{e}^{bT}\left[1-{\left(\frac{T-{z}_i}{\frac{w}{2}}\right)}^2\right] $$$$where the constants a and b are empirically derived values that control the exponential increase of growth rate with temperature and the trait parameters ( z i and w ) control the species‐specific response to temperature. The values for a , the growth rate at 0°C (0.81 day −1 ), and b , the exponential increase in growth rate with temperature (0.0631 day −1 ), are taken from empirical analyses (Bissinger et al., 2008) and are commonly utilized (Smith et al., 2021; Thomas et al., 2012). All model species have the same niche width ( w ; 10°C), which is roughly the niche width of observed North Atlantic phytoplankton species (Irwin et al., 2012).…”

“…for each species across all boxes. Using a kernel density estimate allowed for a continuous curve estimate over the finite range of temperatures in the model and made it simple to calculate the maximum and width of the curve without introducing bias via parameterization (Antell et al, 2021;Broennimann et al, 2012;Smith et al, 2021).…”

“…Biotic interactions such as competition and predation should, in theory, lead to narrower realized than fundamental temperature niches (Colwell & Rangel, 2009;Hutchinson, 1957). However, a recent study of Prochlorococcus temperature niches found that realized temperature niches were wider and colder than fundamental temperature niches, as measured in laboratory conditions, for four globally distributed ecotypes (Smith et al, 2021). Prochlorococcus is the most abundant photosynthetic microbe on Earth and is comprised of many ecotypes with distinct traits and biogeographies (Chisholm et al, 1992;Larkin et al, 2016;Rocap et al, 2003;Zinser et al, 2006).…”

Basin-scale biogeography of marine phytoplankton reflects cellular-scale optimization of metabolism and physiology

“…Growth rates and metabolic fluxes were adjusted for temperature effects by comparing in situ growth temperatures to a model of temperature-dependent growth, parameterized for each strain. Our approach provides a strain-specific parameterization while avoiding the effects of adaptive laboratory evolution, which can be substantial (55). First, the Arrhenius activation energy E a was calculated on the basis of growth rates determined in batch cultures of 12 Prochlorococcus strains (9,56).…”