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Autotrophic and heterotrophic microbes in stream biofilms dominate biogeochemical cycling and rely on nutrient and energy resources for growth and productivity. In the boreal forest, variation in these resources can originate from permafrost distribution and controls competition for nutrients between stream autotrophs and heterotrophs. We investigated which resources control nutrient uptake and metabolism in headwater stream biofilms of subarctic Alaska, USA, and how resource availability affects competition for inorganic nutrients. We hypothesized that the competitive outcome between autotrophs and heterotrophs for inorganic nutrients would be dependent on availability of organic C, or inorganic nutrients (N and P). To test our hypotheses, we measured resource limitation at the patch and reach scales along a permafrost gradient in interior Alaska. At the patch scale, nutrient diffusing substrata revealed that, secondary to light, N and P were colimiting to autotrophic growth, whereas C was primarily limiting to heterotrophic respiration. In the presence of labile C, heterotrophs exhibited a larger response to nutrient enrichment and outcompeted autotrophs for inorganic nutrients. At the reach scale, light availability had the largest influence on nutrient uptake, but inorganic nutrients were also important. The positive response to increased nutrient and C availability at the patch scale suggests that the predicted increase in exports into fluvial networks with permafrost degradation will alter biofilm structure and function. Ultimately, biofilm communities will shift to more heterotroph-dominated patches if heterotrophs outcompete autotrophs for inorganic nutrients. As permafrost thaws and nutrients and organic C mobilize into streams, nutrient uptake dynamics and competition within biofilms will be altered, affecting nutrient use and export.
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Mixotrophy in nanoflagellates across environmental gradients in the ocean
Mixotrophy, the combination of autotrophic and heterotrophic nutrition, is a common trophic strategy among unicellular eukaryotes in the ocean. There are a number of hypotheses about the conditions that select for mixotrophy, and field studies have documented the prevalence of mixotrophy in a range of environments. However, there is currently little evidence for how mixotrophy varies across environmental gradients, and whether empirical patterns support theoretical predictions. Here I synthesize experiments that have quantified the abundance of phototrophic, mixotrophic, and heterotrophic nanoflagellates, to ask whether there are broad patterns in the prevalence of mixotrophy (relative to pure autotrophy and heterotrophy), and to ask whether observed patterns are consistent with a trait-based model of trophic strategies. The data suggest that mixotrophs increase in abundance at lower latitudes, while autotrophs and heterotrophs do not, and that this may be driven by increased light availability. Both mixotrophs and autotrophs increase greatly in productive coastal environments, while heterotrophs increase only slightly. These patterns are consistent with a model of resource competition in which nutrients and carbon can both limit growth and mixotrophs experience a trade-off in allocating biomass to phagotrophy vs. autotrophic functions. Importantly, mixotrophy is selected for under a range of conditions even when mixotrophs experience a penalty for using a generalist trophic strategy, due to the synergy between photosynthetically derived carbon and prey-derived nutrients. For this reason mixotrophy is favored relative to specialist strategies by increased irradiance, while at the same time increased nutrient supply increases the competitive ability of mixotrophs against heterotrophs.
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- Award ID(s):
- 1559356
- PAR ID:
- 10224820
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 116
- Issue:
- 13
- ISSN:
- 0027-8424
- Page Range / eLocation ID:
- 6211 to 6220
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Key Points Warming results in increased productivity, but decreased biomass, in marine microbial food webs due to the thermal dependence of metabolism Higher temperatures disproportionately favor higher trophic levels, increasing the ratio of heterotrophs to autotrophs Thermal responses are amplified if heterotrophic and autotrophic processes have different temperature sensitivity coefficientsmore » « less
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Abstract In oligotrophic oceans, the smallest eukaryotic phytoplankton are both significant primary producers and predators of abundant bacteria such asProchlorococcus. However, the drivers and consequences of community dynamics among these diverse protists are not well understood. Here, we investigated how trophic strategies along the autotrophy‐mixotrophy spectrum vary in importance over time and across depths at Station ALOHA in the North Pacific Subtropical Gyre. We combined picoeukaryote community composition from a 28‐month time‐series with traits of diverse phytoplankton isolates from the same location, to examine trophic strategies across 13 operational taxonomic units and 8 taxonomic classes. We found that autotrophs and slower‐grazing mixotrophs tended to prevail deeper in the photic zone, while the most voracious mixotrophs were relatively abundant near the surface. Within the mixed layer, there was greater phagotrophy when conditions were most stratified and when Chlaconcentrations were lowest, although the greatest temporal variation in trophic strategy occurred at intermediate depths (45–100 m). Dynamics at this site are consistent with previously described spatial patterns of trophic strategies. The success of relatively phagotrophic phytoplankton at shallower depths in the most stratified waters suggests that phagotrophy is a competitive strategy for acquiring nutrients when energy from light is plentiful.more » « less
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The Argo Basin of the eastern Indian Ocean in austral summer (February 2022) was characterized by warm (28.5–30.6 ◦C), oligotrophic surface waters (nitrate and phosphate ≤0.1 μM), with relatively shallow mixed layers and deep chlorophyll biomass maxima. From euphotic zone depth-resolved samples analyzed by for DNA and acid vacuole staining (Hoechst and LysoTracker Green) by ship-board flow cytometry, we found that autotrophic populations were dominated by Prochlorococcus, followed by mixotrophs (58 and 28 % of autotrophic community biomass, respectively), with only 14 % obligate phototrophic phytoplankton (i.e., plastidic cells without acid vacuole fluorescence). Acid vacuole-containing microbes (mixotrophs and heterotrophs) were 34 % of the microbial community, and 80 % of the eukaryotic biomass. In shallow waters, the eukaryotic chlorophyllcontaining community was comprised of pico-sized obligate phototrophs and mixotrophs (233–325 cells mL−1), nano-sized obligate phototrophs and mixotrophs (72 and 374 cells mL−1, respectively), with all groups increasing several-fold in the deep chlorophyll maxima. Mixotrophs were a higher proportion of the chlorophyll-containing community in the shallow nutrient-poor mixed layer, consistent with a nutrient-acquisition argument for their prevalence. Heterotrophic eukaryotes averaged 524 ± 36 cells mL−1 in the euphotic zone, changing little with depth and showing a significant positive relationship with Prochlorococcus, but not any other group. In contrast, mixotrophs were positively correlated with heterotrophic bacteria, but not with Prochlorococcus. Overall, the high proportion of mixotrophs in the microbial community may channel more productivity to higher trophic levels than expected given the region’s nutrient-poor status.more » « less
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Prey removal incubations were conducted in the Argo Basin (eastern Indian Ocean) to investigate the trophic ecology of the zooplankton community supporting Southern Bluefin Tuna larvae. Copepod grazing and selectivity were evaluated considering prey trophic mode and size as food quality descriptors and compared with microzooplankton grazing. Copepods ingested between 3.4 and 138 ng carbon (C) ind−1 d−1. Diet was dominated by mixotrophic (5–89 %) and heterotrophic (0–84 %) prey, with autotrophs contributing 2–17 %. Nanoplankton provided the highest C intake to copepods (62–99 %) versus picoplankton (0.8–38 %), despite more picoplankton cells ingested. No measurable reduction in chlorophyll a (Chla) concentration occurred from copepod grazing through food removal, suggesting an indirect trophic pathway, although gut content revealed ingestion of 0.8 μg Chla ind−1 d−1. Calculations from disappearance incubations imply copepod selection on picoplankton (E = 0.3) over nanoplankton, but picoplankton were likely ingested as aggregates or depressed due to a trophic cascade of copepods ingesting nano-microzooplankton. Copepods ingested protistan consumers and/or metazoans fed on 15N-cyanobacteria with ~5-fold higher N uptake from 1 to 2 μm 15N-Synechococcus than from <1 μm 15NProchlorococcus. Microzooplankton grazing on eukaryotes (0.07–2.5 d−1) and prokaryotes (0.3–2.1 d−1) greatly exceeded copepod grazing. Microzooplankton diet consisted mostly of heterotrophs (25–59 %) and mixotrophs (13–41 %) followed by autotrophs (12–33 %), with more nano- (95–98 %) than picophytoplankton (2–5 %). Overall, microzooplankton removed most daily production (111 %) in contrast to 7 % for copepods. Our findings indicate that mixotrophy, intraguild grazing and nutrient channeling support the food web in this oligotrophic region.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1073/pnas.1814860116
