Heterotrophic nanoflagellate enhancement of bacterial growth through nutrient remineralization in chemostat culture

Abstract

Heterotrophic nanoflagellates are the principal consumers of picoplankton in the ocean. Their role as nutrient remineralizers is also well established. However, the coupled interactions between grazer consumption and prey growth are less well understood. In this work, we demonstrate a tight coupling among flagellate grazing, nitrogen remineralization, and prey growth, resulting in bacterial growth rates averaging 2-to 14-fold higher in the presence of flagellate grazers. These results were obtained using 2-stage, nitrogen-limited chemostats containing a mixed culture of heterotrophic bacteria enriched from seawater and Paraphysomonas bandaiensis, a chrysomonad flagellate. Abundance and biovolume of the flagellates were monitored on a daily basis, as was bacterial abundance. Grazing rates were measured using short-term tracer uptake experiments (fluorescently-labeled bacteria and beads), and these data were used to calculate gross bacterial growth rates in the presence of grazers. A mass balance approach was used to estimate reduced nitrogen regenerated by the protist and nitrogen demand of the heterotrophic bacteria. These independent methods of assessing grazer growth and feeding, coupled with estimates of flagellate gross growth efficiency, provided strong, internally consistent constraints on the estimates of bacterial growth rates in the presence of grazers. Under these culture conditions, P. bandaiensis had a carbon-based gross growth efficiency averaging 28%. This work shows that independently measured grazing rates are essential in protist culture work if system dynamics are to be understood. It also underscores the necessity of including protist remineralization pathways in models if realistic simulations are to be obtained.

Effects of temperature on growth rate and gross growth efficiency of an Antarctic bacterivorous protist

“…However, our isolate has a lower maximal growth rate at 20 1C relative to the The relationship between temperature and growth rate (a) or gross growth efficiency (GGE) (b) for strains of Paraphysomonas spp. observed in this study (K growth rates and GGE from this study), and in published reports for temperate and polar strains (D growth rates and GGE from other studies) (Fenchel, 1982;Caron et al, 1985Caron et al, , 1986Caron et al, , 1991Goldman and Caron, 1985;Goldman et al, 1987;Choi and Peters, 1992;Leadbeater, 1994, 1995;Ishigaki and Sleigh, 2001;John and Davidson, 2001;Delaney, 2003;Fu et al, 2003;Selph et al, 2003). Figure 5a).…”

“…Selph et al (2003) reported extremely low GGEs at 18 1C, which resulted in mean and median estimates in the X15 to 20 1C interval, otherwise the range of mean and median values would have been even narrower: 33-50% and 40-51%, respectively. The mean and median values of GGE thus show no apparent relationship with temperature.…”

“…Although the range of reported values of GGE for two species of Paraphysomonas was quite large from a single study (2%-80%; Selph et al, 2003), the mean and median values for each 5 1C increment of temperature were constrained to a relatively narrow range (mean ¼ 29-50%, median ¼ 25-44%; solid and dashed lines, respectively in Figure 5b). Selph et al (2003) reported extremely low GGEs at 18 1C, which resulted in mean and median estimates in the X15 to 20 1C interval, otherwise the range of mean and median values would have been even narrower: 33-50% and 40-51%, respectively.…”

Importance of the Viral Shunt in Nitrogen Cycling in Synechococcus Spp. Growth in Subtropical Western Pacific Coastal Waters

“…Nanoflagellates, on the other hand, may contribute to the release of DOM compounds that are rich in nutritional elements, including N, P, and Fe, while grazing on bacteria (Noble and Fuhrman 1999;Selph et al 2003;Poorvin et al 2004). Although the contribution to nutrient regeneration by nanoflagellate grazers was excluded in our experiments by our use of 1.0 μm filters to remove nanoflagellates in both treatments, we cannot preclude that all nanoflagellates were eliminated.…”

Evidence for Coupling of the Carbon and Phosphorus Biogeochemical Cycles in Freshwater Microbial Communities

“…There is considerable evidence that eukaryotic microbial communities serve a significant role in fertility of aquatic and terrestrial environments (e.g., Bloem et al, 1989;Adl, 2003;Anderson, 2014b), particularly the contribution of heterotrophic protists such as nanoflagellates that prey on bacteria and promote remineralization of mineral and carbon compounds (e.g., Cole et al, 1977;Clarholm, 1989;Caron, 1994;Selph et al, 2003;Anderson, 2012). Some of this effect can be attributed to nutrient release during phagotrophic feeding, especially in the microbial loop (e.g., Güde, 1985;Caron, 1994).…”