Effect of B-vitamins (B1, B12) and inorganic nutrients on algal bloom dynamics in a coastal ecosystem

Abstract

Vitamins play an integral role in the cellular biochemistry of algae, but the effect of these organic metabolites on the growth and diversity of phytoplankton communities has been poorly studied. We integrated newly developed techniques to directly measure vitamins B 1 and B 12 with field-based amendment experiments to elucidate the role of B-vitamins in phytoplankton population dynamics in coastal marine environments. Two sites on Long Island, New York, USA, were monitored from spring through fall: the tidal Old Fort Pond (OFP) and the brackish Peconic River (PR) estuary. Vitamin B 12 levels were similar between sites (OFP: 1.6 to 21 pM; PR: 1.6 to 17 pM) and were significantly correlated with bacterial densities, dissolved organic nitrogen and dissolved organic phosphorus at OFP, suggesting that B 12 behaves like regenerated organic nutrients. Concentrations of vitamin B 1 were substantially higher in the freshwater dominated site (PR: 12 to 190 pM; OFP: 9 to 43 pM) and were inversely correlated with salinity, suggesting that rivers and groundwater may be an important source of vitamin B 1 . During dinoflagellate blooms (>10 4 cells ml -1), occurring in late summer and early fall, vitamin B 12 and B 1 levels in PR decreased 90% relative to pre-bloom levels, while levels temporarily increased to seasonal maxima in OFP, likely reflecting vitamin synthesis and/or regeneration by microbial communities. Nutrient amendment experiments conducted at both sites during summer demonstrated that algal communities were primarily N-limited, while those conducted during early fall showed that vitamins B 1 and B 12 were each capable of significantly enhancing the biomass of larger phytoplankton (> 5 µm). The autumnal shift in phytoplankton communities from dinoflagellates to diatoms, as vitamin levels became depleted and algal communities were limited by vitamin B 12 , suggests that B-vitamins may influence the succession of coastal phytoplankton. KEY WORDS: B-vitamins · Phytoplankton · Harmful algal blooms · Inorganic nutrients Resale or republication not permitted without written consent of the publisherAquat Microb Ecol 49: [181][182][183][184][185][186][187][188][189][190][191][192][193][194] 2007 1980, Croft et al. 2005). A recent compilation by Croft et al. (2005) indicated that half of the algal species studied in culture (n = 326) cannot grow without an exogenous supply of vitamin B 12 . Sources of vitamins in marine systems include bacterial biosynthesis and allochthonous sources, such as influxes from rivers and streams (Haines & Guillard 1974, Bruno & Staker 1978, Swift 1980. Few studies have examined the effect of ambient vitamin levels on phytoplankton dynamics in marine ecosystems. These studies have generally suggested that vitamins can be present at picomolar concentrations in seawater and may sometimes be depleted to growth-limiting levels (Swift 1980, Croft et al. 2005, Panzeca et al. 2006, Bertrand et al. 2007. Recent independent studies have demonstrated that phytoplankton communities in the S...

Most harmful algal bloom species are vitamin B1and B12auxotrophs

“…Our quantitative results demonstrate that vitamins B 1 and B 12 can limit the accumulation of microalgal biomass over a wide range of concentrations, and that the limiting concentrations for some species in culture are higher than levels present in some coastal waters. For example, the growth of the toxic dinoflagellate Karenia mikimotoi and the "brown tide" species Aureococcus anophagefferens displayed half-saturation constants of 13.1 and 3.49 pM, respectively, for vitamin B 12 (Table 2), which are similar to concentrations typically found in coastal systems (0.5-20 pM) (18,22). In the case of A. anophagefferens, the genomic presence of a vitamin B 12 -dependent methionine synthase (metH) and absence of the vitamin B 12 -independent methionine synthase (metE) confirms its absolute requirement of this vitamin (15).…”

“…Studies measuring vitamin B 12 in the ocean have shown levels are lower than those estimated by prior bioassays (18) and in many cases, concentrations of levels are substantially less than the 7-pM threshold (18) putatively required by many phytoplankton in culture (15). A series of studies have demonstrated that vitamins can stimulate phytoplankton growth in Fe-limited, high-nutrient, low-chlorophyll (HNLC) regions of Antarctica (19,20) and coastal zones where HABs commonly occur (21,22).…”

“…Studies measuring vitamin B 12 in the ocean have shown levels are lower than those estimated by prior bioassays (18) and in many cases, concentrations of levels are substantially less than the 7-pM threshold (18) (15) and field studies, however, have examined a relatively small number of dinoflagellates and very few HAB species (namely, Karenia brevis, Gymnodinium catenatum, Amphidinium operculatum, and Akashiwo sanguinea). Investigations of phytoplankton requirements for vitamins B 1 and B 7 have been exceedingly rare (22,28). Because there exists no discernible evolutionary pattern to vitamin auxotrophy among algae (15, 29), a more comprehensive investigation of the qualitative and quantitative vitamin requirements of HABs is needed to better understand the autoecology of these events.…”

Unraveling Vitamin B12-Responsive Gene Regulation in Algae

“…On the other hand, if there is a reliable and abundant external source of B 12 , and these conditions prevail over a long period of time, the gene may be lost entirely, which is the derived state of many algal species spanning multiple diverse phyla (Croft et al, 2005;Helliwell et al, 2011). However, natural levels of B 12 are reportedly less than 10 ng L 21 (10 pM) in freshwater (Kurata, 1986) and perhaps up to 70 ng L 21 in seawater (Carlucci, 1970;Gobler et al, 2007), with more recent measurements indicating a lower range in the photic zone of the Southern Ocean and North Atlantic Ocean (Panzeca et al, 2009;Sañudo-Wilhelmy et al, 2012). The extracellular concentration of B 12 necessary to repress the METE transcript (Fig.…”

“…Improved methodology for the quantification of thiamine and cobalamin in environmental samples revealed a heterogenous distribution of these vitamins in the oceans, with generally very low levels free in solution in the photic zone (Sañudo-Wilhelmy et al, 2012). It has also been shown, through fertilization experiments, that vitamins are limiting for algal growth in several marine environments (Gobler et al, 2007). Therefore, it is intriguing that many oligotrophic species such as Ostreococcus tauri are nonetheless vitamin auxotrophs (Worden et al, 2009;Helliwell et al, 2011) and so must be able to obtain a ready source of these organic micronutrients from their surroundings.…”