Regulation of growth and toxicity of a mixotrophic microbe: implications for understanding range expansion in Prymnesium parvum

Abstract

The rapid range expansion of the toxigenic marine haptophytic alga Prymnesium parvum in inland aquatic systems across the southern USA and beyond has prompted great interest in the ecology and evolutionary biology of this invasive bloom-forming species. Researchers have speculated that increased toxicity and heterotrophy in suboptimal environments allow blooms to develop in these new inland habitats that seem to represent extremes relative to P. parvum's perceived optimal niche. We used a laboratory-based study to elucidate the roles of salinity and nutrient availabilities in P. parvum growth and toxicity under environmental conditions representative of hypereutrophic reservoirs of the southwestern USA in which P. parvum blooms are now common. We found evidence that nutrient conditions favoring toxigenesis in P. parvum are suboptimal for growth and bloom formation, whereas conditions conducive to high growth rates are less favorable for toxigenesis. In contrast, both growth and toxicity scaled positively with salinity. Taken in the context of the documented biogeography of P. parvum and that toxigenesis in P. parvum probably evolved in support of heterotrophic nutrient acquisition, our results suggest that P. parvum's apparent range expansion into and across the USA is driven by increasing availabilities of salty and nutrient-rich systems, rather than by its toxigenic abilities.

The niche of an invasive marine microbe in a subtropical freshwater impoundment

“…Not only were P. parvum growth rates during blooms in Lebanon Pool, Lake Texoma (Oklahoma-Texas) negatively related to temperatures between 7 1C and 16 1C, these blooms were large (up to 200 000 cells per ml) and quite toxic, as indicated by bioassays and large fish kills Zamor et al, 2014). In Hambright et al (2014), both growth rates and general toxicity in cultures were found to increase with increasing salinity.…”

“…Because it is a microbial eukaryote that can occur in immense numbers, encyst and be passively transported, P. parvum's dispersal capabilities are potentially unlimited (sensu Finlay, 2002; but see Martiny et al, 2006;Hanson et al, 2012) and subjected to probabilities related to various potential vectors, such as wind, migratory-animal-assisted propagation or even human intervention (Johnson et al, 2008). For example, Hambright et al (2014) estimated that during a P. parvum bloom of 10 5 cells per ml in Lebanon Pool (volume B3 Â 10 6 m 3 ), the total P. parvum population would exceed 3 Â 10 11 individuals and represent an immense pool for downstream transport of invasive propagules via hydraulic flushing and advective downstream flow. Yet, P. parvum, which is often detected downstream, has yet to bloom in any area of the lake outside the environmental conditions identified here (Zamor et al, 2012).…”

“…This apparent incredible range expansion since the first North American report (Pecos River of southern Texas) in the 1980s (James and De La Cruz, 1989) represents an interesting enigma-while P. parvum has an ability to thrive across a broad range of environmental conditions (Edvardsen and Paasche, 1998), the conditions found in most North American bloom sites tend to be far removed from optimal conditions described from the laboratory study (Baker et al, 2009). Most inland blooms of P. parvum in the southwestern United States have occurred at relatively low salinities (1-3 partial salinity units, psu) during winters when temperatures range from 10 1C to 20 1C, yet laboratory studies suggest that inland strains of P. parvum are well suited to high salinities (8-30 psu) and temperatures (20-30 1C) (Baker et al, 2007(Baker et al, , 2009Hambright et al, 2010Hambright et al, , 2014Roelke et al, 2011;Patiñ o et al, 2014). This apparent paradox has led to speculation that its toxigenic capabilities provide a competitive edge to P. parvum over other algae, allowing blooms to develop during periods of stress, such as created by low nutrient availabilities (for a review, see Granéli et al, 2012).…”

“…If true, microbial biogeographic distributions may be reflective only of technical limitations in detection, whereas their active or meaningful participation in a community will depend on the suitability of a given habitat to foster positive population growth (Gibbons et al, 2013;Hambright et al, 2014). The marine haptophyte Prymnesium parvum Carter is considered to be a globally invasive species in many freshwater systems in which it is now a community member and often dominant.…”

Dynamics of an experimental microbial invasion

“…Although still presumably subjected to downstream transport of propagules from these large, sustained blooms, which can reach densities over 2 × 10 5 cells per mL, the rest of the lake has not experienced any establishment of P. parvum (defined as recurrent winter blooms). However, it is important to keep in mind that, before propagule exposure, we manipulated our microcosms' salinity levels to mimic those thought to be conducive to P. parvum establishment: i.e., ∼2 ppt (29,41), effectively creating a niche space for P. parvum. The role of salinity is particularly important, P. parvum being a marine species that is already at the limit of its salinity tolerance in this reservoir (41) and with most recorded blooms occurring when salinity exceeds 1.7 practical salinity units (psu) (29).…”