The alkaline phosphatase PhoX is more widely distributed in marine bacteria than the classical PhoA

Abstract

Phosphorus (P) is a vital nutrient for all living organisms and may control the growth of bacteria in the ocean. Bacteria induce alkaline phosphatases when inorganic phosphate (Pi) is insufficient to meet their P-requirements, and therefore bulk alkaline phosphatase activity measurements have been used to assess the P-status of microbial assemblages. In this study, the molecular basis of marine bacterial phosphatases and their potential role in the environment were investigated. We found that only a limited number of homologs to the classical Escherichia coli alkaline phosphatase (PhoA) were present in marine isolates in the Bacteroidetes and γ-proteobacteria lineages. In contrast, PhoX, a recently described phosphatase, was widely distributed among diverse bacterial taxa, including Cyanobacteria, and frequently found in the marine metagenomic Global Ocean Survey database. These taxa included ecologically important groups such as Roseobacter and Trichodesmium. PhoX was induced solely upon P-starvation and accounted for approximately 90% of the phosphatase activity in the model marine bacterium Silicibacter pomeroyi. Analysis of the available transcriptomic datasets and their corresponding metagenomes indicated that PhoX is more abundant than PhoA in oligotrophic marine environments such as the North Pacific Subtropical Gyre. Those analyses also revealed that PhoA may be important when Bacteroidetes are abundant, such as in algal bloom episodes. However, PhoX appears to be much more widespread. Its identification as a gene that mediates organic P acquisition in ecologically important groups, and as a marker of Pi-stress, constitutes an important step toward a better understanding of the marine P cycle.

Subcellular localization of marine bacterial alkaline phosphatases

“…A recent study showed that PhoX is more abundant in the ocean than previously considered (18). We observed that PhoD is even more abundant than PhoX across a wide variety of marine habitats.…”

“…The replacement of Zn 2ϩ with Ca 2ϩ could be an important factor in the selection of PhoX and PhoD over PhoA in the ocean. We applied a loose but reliable searching criterion and identified more PhoA and PhoX homologs than previously shown (18). The abundant nature of PhoD genes suggests that they may play an important role in organophosphate hydrolysis in the surface oceans.…”

“…Moreover, 4 pairs of PhoX and PhoD peptides were mapped to four paired reads and one pair of PhoX and PhoD was mapped to a single read (Dataset S2), indicating that PhoX and PhoD can co-occur in marine bacteria. Both PhoX and PhoD are activated by Ca 2ϩ , an abundant ion in the ocean, whereas PhoA requires Zn 2ϩ (Table S1), which often occurs at subnanomolar concentrations (18,19). The replacement of Zn 2ϩ with Ca 2ϩ could be an important factor in the selection of PhoX and PhoD over PhoA in the ocean.…”

A microarray for assessing transcription from pelagic marine microbial taxa

“…Target genes for oligonucleotide probe design were selected based on existing knowledge of gene markers that target microorganism interactions with their environment (for example, Lindell and Post, 2001;Webb et al, 2001;Holtzendorff et al, 2002;Chen et al, 2004;Fuller et al, 2005;Dyhrman and Haley, 2006;Zehr et al, 2007;Orchard et al, 2009;Sebastian and Ammerman, 2009;Kamennaya and Post, 2011;Mosier and Francis, 2011;Paerl et al, 2011). Several genes for hypothetical proteins that were differentially expressed in response to specific stimuli in cultured marine microorganisms were also included (Scanlan et al, 1996;Martiny et al, 2009;Shi et al, 2009;Tetu et al, 2009; et al, 2011).…”

Interactions of cadmium, zinc, and phosphorus in marine Synechococcus : field uptake, physiological and proteomic studies

“…Alkaline phosphatases (phoA) are thought to be located in the periplasm and are activated by Zn and magnesium, whereas other alkaline phosphatases (phoX, phoD) are activated by calcium ions (Luo et al, 2009). A recent survey of the metagenomic databases concluded that phoX appeared to be more widespread in the ocean than phoA (Sebastian and Ammerman, 2009). There are also other types of alkaline phosphatases in cyanobacteria.…”