Mixotrophy in Heterocapsa rotundata: A mechanism for dominating the winter phytoplankton

Abstract

Heterocapsa rotundata is a mixotrophic dinoflagellate that can ingest picoplankton, including bacteria, and is known to form large blooms in temperate estuaries during wet winters, particularly when grazing pressure on phytoplankton is low. We hypothesized that phagotrophy gives H. rotundata an advantage over other phytoplankton species during low light conditions. We used laboratory and field experiments to investigate changes in phagotrophy by H. rotundata in response to changes in light availability. Prey removal experiments with a non-axenic culture of H. rotundata were used to determine changes in H. rotundata's ingestion rates in response to changes in irradiance. Fluorescent microspheres were used to measure in situ ingestion rates of H. rotundata collected on 20 different occasions from the Choptank River during the winter of 2016. In situ H. rotundata ingestion rates were tested for correlation with inorganic nutrient concentrations and irradiance levels. Ingestion rates measured with cultured and in situ H. rotundata followed similar patterns and ingestion rates increased as irradiance decreased. H. rotundata has the potential to obtain nutrients from multiple nutrient sources, switching from phototrophy to partial heterotrophy as irradiance decreases. This response may allow H. rotundata to survive and to potentially form blooms when growth rates of most other estuarine phytoplankton species is low.Heterocapsa is a genus of dinoflagellates that contains numerous bloom forming and toxic species (Salas et al. 2014). One particular species, Heterocapsa rotundata (Lohmann) Loeblich (Hansen 1995), is ubiquitous and occasionally forms large blooms. H. rotundata has been reported in a range of environments all over the world including Chesapeake Bay, U. . H. rotundata tends to either dominate or be a prominent part of the phytoplankton community for at least part of the year in some of these areas (Seong et al. 2006;Balzano et al. 2015;Millette et al. 2015). Yet, relatively few studies have focused on the ecology of H. rotundata.Some studies have focused on the formation and decline of H. rotundata winter blooms in Chesapeake Bay tributaries (Cohen 1985; Sellner et al. 1991;Millette et al. 2015). These researchers found abundant H. rotundata blooms in wet, cold winters when salinity is low (Cohen 1985) and when there is a release in grazing pressure from microzooplankton and copepods (Millette et al. 2015). Although wet, cold winters and a release in grazing pressure are factors that impact every phytoplankton species, it is unknown how H. rotundata can take advantage of these conditions over other species to bloom. One possibility is that H. rotundata may use their capacity as a mixotroph to overcome light limitation. This would give H. rotundata an advantage over other phytoplankton in the winter. H. rotundata has been shown to consume heterotrophic bacteria, cyanobacteria such as Synechococcus, and small diatoms (Seong et al. 2006;Jeong et al. 2010). Their bacterial ingestion rate is known to incr...

Nutrient- and Climate-Induced Shifts in the Phenology of Linked Biogeochemical Cycles in a Temperate Estuary

“…Winter blooms of dinoflagellates have been documented in the estuarine turbidity maximum region of the main stem Chesapeake Bay, in the vicinity of the CB3.1 (Lee et al, 2012), as well as in multiple tributaries of Chesapeake Bay (Sellner et al, 1991;Millette et al, 2015). Many of these species tend to be mixotrophic, using phagotrophy as an alternative energy acquisition strategy during winter-spring in turbid waters, where low light availability limits photoautotrophy (Millette et al, 2017). The moderate increases in stratification (and presumably lower turbulence) we confirmed during this season in the landward Bay regions would likely favor these small, flagellated organisms (Margalef, 1978;Hinder et al, 2012).…”

Contrasting effects of high‐intensity photosynthetically active radiation on two bloom‐forming dinoflagellates

“…By up‐regulating feeding in response to low light (Millette et al. ) and, as shown here, by optimizing photosynthetic performance under these conditions, H. rotundata appears to gain an advantage over other phytoplankton. In contrast, the bloom niche of Alexandrium fundyense is likely characterized by low turbulence (with associated low shear stress) and much higher light.…”

“…Heterocapsa rotundata has been shown to increase feeding when light is low (Millette et al. ) while predation by many other mixotrophic dinoflagellates is stimulated by light (Hansen and Nielsen , Stoecker et al. , Jakobsen et al.…”

“…In addition, Alexandrium and Heterocapsa are both mixotrophic genera that obtain nutrition from ingested prey as well as photosynthesis (Jeong et al 2005b, Seong et al 2006. Heterocapsa rotundata has been shown to increase feeding when light is low (Millette et al 2017) while predation by many other mixotrophic dinoflagellates is stimulated by light (Hansen and Nielsen 1997, Stoecker et al 1997, Jakobsen et al 2000, Kim et al 2008. It is unknown how high, potentially stressful, irradiances affect this behavior.…”

“…In Chesapeake Bay, Heterocapsa rotundata often blooms in winter when light limits the growth of other phytoplankton and predators are scarce as a result (Cohen 1985, Sellner et al 1991, Millette et al 2015. By up-regulating feeding in response to low light (Millette et al 2017) and, as shown here, by optimizing photosynthetic performance under these conditions, H. rotundata appears to gain an advantage over other phytoplankton. In contrast, the bloom niche of Alexandrium fundyense is 1092 likely characterized by low turbulence (with associated low shear stress) and much higher light.…”