High sequence variability, diverse subcellular localizations, and ecological implications of alkaline phosphatase in dinoflagellates and other eukaryotic phytoplankton.

Xin Lin,Huan Zhang,Senjie Lin,Yudong Cui

doi:10.3389/fmicb.2012.00235

Abstract

Alkaline phosphatase (AP) is a key enzyme for phytoplankton to utilize dissolved organic phosphorus (DOP) when dissolved inorganic phosphorus is limited. While three major types of AP and their correspondingly diverse subcellular localization have been recognized in bacteria, little is known about AP in eukaryotic phytoplankton such as dinoflagellates. Here, we isolated a full-length AP cDNA from a latest-diverging dinoflagellate genus Alexandrium, and conducted comparative analyses with homologs from a relatively basal (Amphidinium carterae) and late-diverging (Karenia brevis) lineage of dinoflagellates as well as other eukaryotic algae. New data and previous studies indicate that AP is common in dinoflagellates and most other major eukaryotic groups of phytoplankton. AP sequences are more variable than many other genes studied in dinoflagellates, and are divergent among different eukaryotic phytoplankton lineages. Sequence comparison to the other characterized APs suggests that dinoflagellates and some other eukaryotic phytoplankton possess the putative AP as phoA type, but some other eukaryotic phytoplankton seem to have other types. Phylogenetic analyses based on AP amino acid sequences indicated that the “red-type” eukaryotic lineages formed a monophyletic group, suggesting a common origin of their APs. As different amino acid sequences have been found to predictably determine different spatial distribution in the cells, which may facilitate access to different pools of DOP, existing computational models were adopted to predict the subcellular localizations of putative AP in the three dinoflagellates and other eukaryotic phytoplankton. Results showed different subcellular localizations of APs in different dinoflagellates and other lineages. The linkage between AP sequence divergence, subcellular localization, and ecological niche differentiation requires rigorous experimental verification, and this study now provides a framework for such a future effort.

Highlights

In marine ecosystem, phosphorus (P) is a vital nutrient controlling the growth of phytoplankton thereby affecting primary production (Karl, 2000; Paytan and McLaughlin, 2007)
The Alkaline phosphatase (AP) sequences are moderately conserved among three dinoflagellates (48–52% identical or 63–66% chemically similar at the aa level) and the overall characteristics are similar (Table 1, Figure 1A)
AP activity has not been detected in raphidophytes, and the AP gene has not been identified in the genomes of rhodophytes, such as Cyanidioschyzon merolae (Table S2 in Supplementary Material)

Summary

Introduction

Phosphorus (P) is a vital nutrient controlling the growth of phytoplankton thereby affecting primary production (Karl, 2000; Paytan and McLaughlin, 2007). DIP is preferable for the growth of phytoplankton; its concentration is often so low that it limits phytoplankton growth in marine environments (BenitezNelson, 2000; Karl, 2000; Dyhrman et al, 2006; Meseck et al, 2009). In various areas of the open ocean, DIP occurs in nanomolar concentrations (Wu et al, 2000; Thingstad et al, 2005) and has been shown to be a limiting or co-limiting factor of nitrogen fixation (Sañudo-Wilhelmy et al, 2001; Mills et al, 2004) and primary production (Paytan and McLaughlin, 2007). DIP can be stoichiometrically limited by high amounts of nitrogen associated with human activities (Cloern, 2001; Huang et al, 2003; Scavia and Bricker, 2006; Zhang et al, 2007c). Eutrophication with stoichiometric DIP limitation can potentially impose coastal health problems because some harmful algal bloom forming species, such as Alexandrium spp., Dinophysis acuminate, Karlodinium veneficum, and Pseudo-nitzschia multiseries can elevate their toxin production under P-limited conditions (Anderson et al, 2002; John and Flynn, 2002; Fu et al, 2010; Mooney et al, 2010)

Methods

Results

Discussion

Conclusion