The ISME Journal (2015) 9, 256–264 & 2015 International Society for Microbial Ecology All rights reserved 1751-7362/15 www.nature.com/ismej ORIGINAL ARTICLE The niche of an invasive marine microbe in a subtropical freshwater impoundment K David Hambright1,2,3, Jessica E Beyer1,2, James D Easton1,3, Richard M Zamor1,2, Anne C Easton1,3 and Thayer C Hallidayschult1,2 1Plankton Ecology and Limnology Laboratory, Department of Biology, University of Oklahoma, Norman, OK, USA; 2Program in Ecology and Evolutionary Biology, Department of Biology, University of Oklahoma, Norman, OK, USA and 3Biological Station, Department of Biology, University of Oklahoma, Norman, OK, USA Growing attention in aquatic ecology is focusing on biogeographic patterns in microorganisms and whether these potential patterns can be explained within the framework of general ecology. The long-standing microbiologist’s credo ‘Everything is everywhere, but, the environment selects’ suggests that dispersal is not limiting for microbes, but that the environment is the primary determining factor in microbial community composition. Advances in molecular techniques have provided new evidence that biogeographic patterns exist in microbes and that dispersal limitation may actually have an important role, yet more recent study using extremely deep sequencing predicts that indeed everything is everywhere. Using a long-term field study of the ‘invasive’ marine haptophyte Prymnesium parvum, we characterize the environmental niche of P. parvum in a subtropical impoundment in the southern United States. Our analysis contributes to a growing body of evidence that indicates a primary role for environmental conditions, but not dispersal, in the lake- wide abundances and seasonal bloom patterns in this globally important microbe. The ISME Journal (2015) 9, 256–264; doi:10.1038/ismej.2014.103; published online 20 June 2014 Introduction notion of the rare or dormant microbial biosphere in microbes (Sogin et al., 2006; Caron and Countway, ‘Everything is everywhere, but, the environment 2009; Jones and Lennon, 2010; Gibbons et al., 2013), selects’ (Baas-Becking, 1934; de Wit and Bouvier, and leads to the hypothesis that environmental 2006) suggests that dispersal is not limiting for conditions that foster high growth in P. parvum microbes, but that the environment is the primary relative to other microbial constituents are the factor determining whether a particular microbe is principle determinants of P. parvum blooms in actively participating in a given community. If true, inland freshwater systems. microbial biogeographic distributions may be reflec- P. parvum blooms and fish kills have been tive only of technical limitations in detection, observed in many inland aquatic systems world- whereas their active or meaningful participation in wide (Grane´li et al., 2012), including waterbodies, a community will depend on the suitability of a mostly reservoirs, in at least 20 US states (Roelke given habitat to foster positive population growth et al., 2011; Hambright, 2012). This apparent (Gibbons et al., 2013; Hambright et al., 2014). The incredible range expansion since the first North marine haptophyte Prymnesium parvum Carter is American report (Pecos River of southern Texas) in considered to be a globally invasive species in many the 1980s (James and De La Cruz, 1989) represents freshwater systems in which it is now a community an interesting enigma—while P. parvum has an member and often dominant. However, recent study ability to thrive across a broad range of environ- has suggested that P. parvum is not dispersal mental conditions (Edvardsen and Paasche, 1998), limited, as extremely low-density populations have the conditions found in most North American bloom been detected in habitats that do not experience sites tend to be far removed from optimal conditions P. parvum blooms, many of which are directly described from the laboratory study (Baker et al., downstream of P. parvum bloom sites (Zamor 2009). Most inland blooms of P. parvum in the et al., 2012). This phenomenon reflects the general southwestern United States have occurred at rela- tively low salinities (1–3 partial salinity units, psu) during winters when temperatures range from 10 1C Correspondence: KD Hambright, Department of Biology, to 20 1C, yet laboratory studies suggest that inland University of Oklahoma, 730 Van Vleet Oval, Norman, OK strains of P. parvum are well suited to high salinities 73072, USA. 1 E-mail: [email protected] (8–30 psu) and temperatures (20–30 C) (Baker et al., Received 22 March 2014; revised 9 May 2014; accepted 13 May 2007, 2009; Hambright et al., 2010, 2014; Roelke 2014; published online 20 June 2014 et al., 2011; Patin˜ o et al., 2014). This apparent Niche of invasive marine microbe in fresh water KD Hambright et al 257 paradox has led to speculation that its toxigenic extremely large watershed (watershed area: lake capabilities provide a competitive edge to P. parvum surface area ¼ 243), nutrient loading to the lake is over other algae, allowing blooms to develop during high and the lake is eutrophic to hypertrophic, periods of stress, such as created by low nutrient depending on season and location within this availabilities (for a review, see Grane´li et al., 2012). complex, dendritic reservoir (Oklahoma Water However, while toxicity may have important roles in Resources Board, 2010). The watershed also con- predator avoidance and heterotrophy in this uni- tains abundant deposits of calcium carbonate, cellular mixotroph, toxin production is unlikely to halite, gypsum, anhydrite and other Permian-Salado provide a competitive advantage to P. parvum to the evaporites (Ground and Groeger, 1994), which lead degree necessary to lead to bloom formation under to salinities that often exceed 1 psu (defined here as suboptimal environmental conditions (Jonsson having a specific conductivity equivalent to 1 g l À 1 et al., 2009; Remmel and Hambright, 2012). NaCl), the general limit for fresh water. The Because it is a microbial eukaryote that can occur phytoplankton are often dominated by filamentous in immense numbers, encyst and be passively and colonial cyanobacteria and the lake is home to a transported, its dispersal capabilities are potentially diverse array of zooplankton, including multiple unlimited (sensu Finlay, 2002; but see Martiny et al., daphniids, numerous copepod and rotifer species 2006; Hanson et al., 2012). Indeed, examination of (Franks et al., 2001; Hambright et al., 2010), and the P. parvum distribution in Lake Texoma (Okla- more than 50 fish species, many of which are homa–Texoma) reveals that P. parvum is dispersed recreationally important (Matthews et al., 2004). throughout the lake, yet blooms and fish kills are common only in areas in which environmental conditions are conducive for growth (Hambright Lake sampling et al., 2010; Zamor et al., 2012). Thus, the recent We sampled eight littoral sites along the northern expansion of P. parvum into new habitats, which is Oklahoma side of Lake Texoma in marinas and typically noted only after a bloom and fish kill, coves, and five pelagic stations in the Red and suggests that habitats with suitable environmental Washita River arms of the lake, as well as at the dam conditions (e.g., elevated nutrients and salinities, (Figure 1). Littoral samples were taken in shallow see below) may be becoming more abundant, (usually o1 m) waters, usually from boat ramps or particularly in the southwestern United States, docks, if present. Temperature and salinity (as where quality of surface water resources is subjected specific conductance), and dissolved oxygen, chlor- to the pressures of climate change and increasing ophyll and phycocyanin concentrations were mea- freshwater demands that accompany growing sured in situ with YSI and Hydrolab sondes, using a human populations and development (Roelke single mid-water point for littoral sites, and surface- et al., 2011). to-bottom water column profiles for pelagic sites. Here we report results of a long-term study of Water samples (1 l; mid-water samples for littoral P. parvum in subtropical Lake Texoma (Oklahoma– sites or 6 to 10 m, depending on depth, integrated Texas, USA), in which P. parvum blooms are now samples for pelagic sites) were collected in acid- commonplace. We use these data to test the washed, deionized- and sample-rinsed Nalgene hypothesis that environmental conditions that foster bottles, stored on ice in the field and refrigerated high growth in P. parvum are the principle determi- in the laboratory for subsequent analyses of nants of P. parvum blooms in the lake. Our analysis P. parvum abundances by quantitative PCR (Zamor provides further support for the Baas-Becking et al., 2012) (microscopy (hemocytometer, 6–12 hypothesis ‘Everything is everywhere, but, the fields per sample) was used in 2006–2007), and for environment selects’, as we identify a primary role concentrations of chlorophyll (acetone extraction), for environmental conditions, but not dispersal, in total nitrogen (TN) and total phosphorus (TP) (flow- the lake-wide distributions and bloom patterns in injection autoanalysis) (American Public Health P. parvum. Association, 1998) and pH. Lake surface elevation data were taken from the 0800 hours measurements recorded at the Denison Dam (Army Corps of Materials and methods Engineers–Tulsa District, 2012). Further details of sampling and sample analyses and additional para- Study site meters monitored can be found in Hambright et al. Lake Texoma (Figure 1), an impoundment of the Red (2010). and Washita Rivers, was constructed in 1944 for flood control, hydropower generation and recrea- tion. The lake is the 12th largest reservoir in the Statistical analyses United States (at normal pool elevation) with a All statistical analyses were carried out in R (version surface area of 360 km2, and mean and maximum 3.0.2; R Development Core Team, 2013). We used depths of 8.7 and 26 m. The lake watershed occupies logistic regression analysis to examine relationships 87 500 km2 of the high plains of Texas and the rolling between Prymnesium distributions within the plains of Texas and Oklahoma.