Most harmful algal bloom species are vitamin B₁and B₁₂auxotrophs

Abstract

Eutrophication can play a central role in promoting harmful algal blooms (HABs), and therefore many HAB studies to date have focused on macronutrients (N, P, Si). Although a majority of algal species require exogenous B vitamins (i.e., auxotrophic for B vitamins), the possible importance of organic micronutrients such as B vitamins (B 1 , B 7 , B 12 ) in regulating HABs has rarely been considered. Prior investigations of vitamins and algae have examined a relatively small number of dinoflagellates (n = 26) and a paucity of HAB species (n = 4). In the present study, the vitamin B 1 , B 7 , and B 12 requirements of 41 strains of 27 HAB species (19 dinoflagellates) were investigated. All but one species (two strains) of harmful algae surveyed required vitamin B 12 , 20 of 27 species required B 1 , and 10 of 27 species required B 7 , all proportions higher than the previously reported for non-HAB species. Half-saturation (K s ) constants of several HAB species for B 1 and B 12 were higher than those previously reported for other phytoplankton and similar to vitamin concentrations reported in estuaries. Cellular quotas for vitamins suggest that, in some cases, HAB demands for vitamins may exhaust standing stocks of vitamins in hours to days. The sum of these findings demonstrates the potentially significant ecological role of B-vitamins in regulating the dynamics of HABs.H armful algal blooms (HABs) are a significant threat to coastal ecosystems, public health, economies, and fisheries, and there are strong links between nutrient loading and HABs within ecosystems around the world (1-3). Most studies of HABs focused on nutrients have primarily investigated the importance of macronutrients (N, P, Si) (2, 3). In contrast, the importance of coenzymes and particularly vitamins (vitamins B 1 , B 7 , and B 12 ) in regulating and stimulating HABs has rarely been considered. This omission is despite the fact that exogenous B vitamins are essential compounds for phytoplankton species that lack the required biosynthetic pathways to produce B vitamins, i.e., vitamin B-auxotrophy (4-10).Vitamin B 12 is essential for the synthesis of amino acids, deoxyriboses, and the reduction and transfer of single carbon fragments in many biochemical pathways (11, 12), whereas vitamin B 1 (thiamine) plays a pivotal role in intermediary carbon metabolism and is a cofactor for number of enzymes involved in primary carbohydrate and branched-chain amino acid metabolism (13,14). More than half of 326 algal species surveyed are auxotrophs for B 12 (10-12, 15) and more than 20% of the 306 microalgal species surveyed are auxotrophs for B 1 [compiled in Croft et al. (14)]. In addition, 5% of 306 algae surveyed require biotin (vitamin B 7 ), a cofactor of several essential carboxylase enzymes, such as acetyl CoA (14).Recently, there has been burgeoning interest in the ability of vitamins to regulate phytoplankton community growth and structure. Novel high performance liquid chromatography (HPLC) techniques for the direct measurement of vitamins B 1 and...

Proteorhodopsin light-enhanced growth linked to vitamin-B1 acquisition in marine Flavobacteria

“…The light stability of vitamin-B 1 is consistent with the use of an artificial white light source in our experiments, as vitamin-B 1 light degradation has been observed only under x-rays, gamma rays and UV irradiation (Gubler, 1984). Vitamin-B 1 concentrations in the growth medium were within the threshold levels considered limiting for some phytoplankton species (Carlucci and Silbernagel, 1966;Tang et al, 2010;Paerl et al, 2015), suggesting that bacteria could have been vitamin-B 1 -deficient during our experiments.…”

Effect of vitamins B1 and B12 on bloom dynamics of the harmful brown tide alga, Aureococcus anophagefferens (Pelagophyceae)

“…A. anophagefferens, strain CCMP1984, was isolated in 1986 from Great South Bay, New York, on Long Island's south shore, and was made axenic and publicly available in 2003. Its vitamin auxotrophy has been previously confirmed in culture and via genomic sequencing (Tang et al 2010;. Cultures obtained from Provasoli-Guillard National Center for Marine Algae and Microbiota were grown in GSe medium (Tang et al 2010) made with artificial salts with and without the addition of B vitamins.…”

“…B vitamins have been found to limit the accumulation of phytoplankton biomass in estuaries where blooms of A. anophagefferens frequently occur (e.g., Quantuck Bay, New York; Sañ udo-Wilhelmy et al 2006). Furthermore, recent laboratory experiments (Tang et al 2010) demonstrated that A. anophagefferens is auxotrophic with respect to both vitamins B 1 and B 12 , a finding confirmed by the presence of genes for B 12 -dependent methionine synthase (metH), but not the B 12 -independent homolog (metE) in its recently sequenced genome Helliwell et al 2011). No field study, however, has investigated the role of B vitamins in HAB events, including brown tides caused by A. anophagefferens, in .…”

Multiple B-vitamin depletion in large areas of the coastal ocean

“…This inference was based on the fact that many species of eukaryotic phytoplankton require vitamins when they are cultured in the laboratory (3)(4)(5)(6)(7). Although it was thought that marine prokaryotes were the major producers of vitamins in the sea (4), genomic data indicate that it is common for both eukaryotic phytoplankton and bacterioplankton to be auxotrophic for at least one B vitamin, mainly because they lack the complete biosynthetic pathways required to produce them (8).…”