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Mixotrophy in Nanoflagellates Across Environmental Gradients in the Ocean

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Mixotrophy in Nanoflagellates Across Environmental Gradients in the Ocean Mixotrophy in nanoflagellates across environmental SEE COMMENTARY gradients in the ocean Kyle F. Edwardsa,1 aDepartment of Oceanography, University of Hawai‘iatManoa, Honolulu, HI 96822 Edited by David M. Karl, University of Hawai‘iatManoa, Honolulu, HI, and approved January 18, 2019 (received for review August 28, 2018) Mixotrophy, the combination of autotrophic and heterotrophic that constrain mixotrophic performance, and food web structure. nutrition, is a common trophic strategy among unicellular eukaryotes For example, Ward et al. (11) assumed that nutrient uptake and in the ocean. There are a number of hypotheses about the conditions phagotrophy are mutually limited by cell surface area and found that select for mixotrophy, and field studies have documented the that mixotrophs competing with autotrophs and heterotrophs prevalence of mixotrophy in a range of environments. However, can persist only when nutrient uptake and prey capture are there is currently little evidence for how mixotrophy varies across diffusion-limited, as opposed to transport-limited. Irradiance environmental gradients, and whether empirical patterns support may also play a key role in the prevalence of mixotrophy, because theoretical predictions. Here I synthesize experiments that have with ample carbon obtained through photosynthesis (relative to quantified the abundance of phototrophic, mixotrophic, and hetero- grazing) a mixotroph may suppress prey density below a spe- trophic nanoflagellates, to ask whether there are broad patterns in cialist heterotroph’s requirements (12). This prediction has been the prevalence of mixotrophy (relative to pure autotrophy and supported by laboratory competition experiments (10, 12, 13) heterotrophy), and to ask whether observed patterns are consistent and may explain why trophic strategies vary with depth in lakes with a trait-based model of trophic strategies. The data suggest that (12). Berge et al. (14) combined nutrient and carbon limitation mixotrophs increase in abundance at lower latitudes, while autotrophs in a trait-based model, assuming that cellular biomass is allo- and heterotrophs do not, and that this may be driven by increased light cated to photosynthesis, nutrient uptake, or phagotrophy, and availability. Both mixotrophs and autotrophs increase greatly in pro- found that mixotrophs achieve higher growth rates than spe- ductive coastal environments, while heterotrophs increase only slightly. cialists during stratified summer conditions when light and prey ECOLOGY These patterns are consistent with a model of resource competition in are relatively abundant but dissolved nutrients are scarce. This which nutrients and carbon can both limit growth and mixotrophs prediction is consistent with the prevalence of autotrophic diatoms experience a trade-off in allocating biomass to phagotrophy vs. during the spring and mixotrophic dinoflagellates during the autotrophic functions. Importantly, mixotrophy is selected for under a summer in the North Atlantic (15). Some models have also in- range of conditions even when mixotrophs experience a penalty for cluded competition for nutrients between mixotrophs and smaller using a generalist trophic strategy, due to the synergy between bacteria or cyanobacteria, which the mixotrophs also consume; photosynthetically derived carbon and prey-derived nutrients. For this under these conditions higher nutrient supply can benefit the reason mixotrophy is favored relative to specialist strategies by intraguild predator (the mixotroph) over its prey (16–18). increased irradiance, while at the same time increased nutrient supply Currently there are few tests of the environmental conditions increases the competitive ability of mixotrophs against heterotrophs. that favor mixotrophy in the ocean, largely due to the difficulty of quantifying the abundance of mixotrophs in natural communities. phytoplankton | microbial | grazing | trait-based model | resource ratio In this study I synthesize experiments from marine systems that aimed to quantify the abundance of mixotrophic nanoflagellates ixotrophy, the combination of autotrophic and heterotro- Mphic nutrition, is an important trophic strategy in plank- Significance tonic microbes (1). A common mode of mixotrophy is phagotrophic predation by photosynthetic eukaryotes (phytoplankton), and for Many single-celled photosynthesizers can also consume other brevity I will refer to phagotrophy by phytoplankton as “mixotrophy.” organisms, a trophic strategy known as mixotrophy. It has Studies over the past several decades have shown that mixotrophs are become clear that mixotrophs are widespread in the ocean, but important consumers in a variety of marine ecosystems, ranging from we know less about the environmental conditions under which low to high latitudes and coastal to open-ocean environments (2–6). they thrive, and whether their abundance is driven by com- These studies also found that mixotrophs cooccur with similar-sized petition with more specialized autotrophs and heterotrophs. autotrophs and heterotrophs. The consequences of mixotrophy for Here it is shown that the major limiting resources for photo- community and ecosystem dynamics are poorly understood, but it synthesis, light and nutrients, likely drive mixotroph success has been proposed that mixotrophy may increase carbon fixation, across different ocean environments. This interpretation of the increase the transfer of organic matter to higher trophic levels, data is supported by a model in which organisms are con- increase nutrient retention in ecosystems, increase the magnitude strained to allocate their biomass among autotrophic and of the biological carbon pump, and suppress the abundance of heterotrophic functions, and the success of trophic strategies is prokaryotes (1, 7–10). determined by the availability of light, nutrients, and prey. Mixotrophy can be conceptualized as a strategy of trophic generalism, relative to the specialized strategies of autotrophy Author contributions: K.F.E. designed research, performed research, analyzed data, and (e.g., diatoms) or heterotrophy (e.g., heterotrophic dinoflagellates). wrote the paper. Because mixotrophs compete with autotrophs for nutrients and The author declares no conflict of interest. light, and compete with heterotrophs for prey, it is important to This article is a PNAS Direct Submission. understand the conditions under which a generalist mixotrophic Published under the PNAS license. strategy is favored relative to specialist strategies, and under See Commentary on page 5846. what conditions multiple strategies can coexist. Theoretical 1Email: [email protected]. studies have addressed these questions using a variety of ap- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. proaches and have produced a variety of predictions, in part due 1073/pnas.1814860116/-/DCSupplemental. to different assumptions about limiting factors, the trade-offs Published online February 13, 2019. www.pnas.org/cgi/doi/10.1073/pnas.1814860116 PNAS | March 26, 2019 | vol. 116 | no. 13 | 6211–6220 Downloaded by guest on September 27, 2021 that consume bacteria (MNF), as well as heterotrophic and 1.0 phototrophic nanoflagellates (HNF and PNF). Bacterivorous flagellates play a key role in microbial food webs, because they link bacterial consumers of dissolved organic matter to higher trophic levels, contribute significantly to nutrient remineralization, 0.8 and graze the picocyanobacteria that are major primary pro- ducers in oligotrophic systems (19). First I ask whether the abundance of MNF/HNF/PNF vary systematically across major 0.6 environmental gradients. I then develop a trait-based model that combines elements of previous work and analyze the model using coexistence theory to understand the mechanistic basis of the observed patterns. 0.4 Results Mixotroph Relative Abundance. Mixotrophs were present and Proportion mixotroph ingestion 0.2 moderately abundant in all studies, suggesting that mixotrophic strategies can coexist with specialists under most conditions. The median ratio of MNF to HNF was 0.17, and the first and third quartiles were 0.07 and 0.44, respectively. The median ratio of 0.0 MNF to ANF was 0.07, and the first and third quartiles were = 0.03 and 0.16, respectively (ANF autotrophic nanoflagellates, 0.0 0.2 0.4 0.6 0.8 1.0 defined as PNF – MNF). These numbers are likely to be un- derestimates, because counts of MNF depend on the mixotrophs Proportion mixotroph abundance ingesting the chosen prey proxy. Some insight into the degree of underestimation can be gained by comparing mixotroph abun- Fig. 1. Proportion mixotroph ingestion vs. proportion mixotroph abun- dance to the mixotroph grazing contribution. The mixotroph dance. Some experiments that estimated abundance of MNF and HNF also contribution to total phagotroph abundance is strongly corre- estimated the total bacterial ingestion by MNF and HNF. Plotted here is the proportion of total ingestion attributed to MNF vs. the proportion of total lated with the mixotroph contribution to total ingestion (R2 = phagotroph abundance attributed to MNF [i.e., MNF/(MNF + HNF)]. The 0.83), but the estimated contribution to abundance tends to be ∼ proportion mixotroph ingestion tends to be greater than the proportion lower by a factor of 1.7 (Fig. 1). Under the assumption that abundance, because ingestion is quantified for both MNF and HNF using la- mixotrophs have the same per capita grazing rate as hetero- beled prey, while for abundance
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