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Sundareshwar, Lakshminarayan M Does sulfation of Didymo stalks facilitate iron adsorption and phosphorus concentration in mats? P. V. Sundareshwar, Lakshminarayan M. Iyer, L. Aravind, L. Kunza, S. Gautam and C. Sandvik. The Didymo Problem The paradox of Didymosphenia geminata: how do high growth rates occur in low nutrient rivers? LIGHT (% of ambient) Adapted from Bothwell and Kilroy 2011 AMBIENT WATER 5 mg.m-3 50 mg.m-3 Kilroy and Bothwell 2011 Role of Stalks Adhesion Structural Access to light Access to nutrients (P) 14 days - NUTRIENT 14 days – After termination Sulfated Polysaccharides Kilroy and Bothwell 2012 Sulfotransferases Sulfotransferases belong to the P-loop kinase superfamily and can be distinguished by conserved sequence and structure features Walker A motif Diatom genomes have a large number of sulfotransferases Protein sequence Databases Output Queries Sequence/Profile search programs Non-redundant database@NCBI, Sulfotransferase HMMER Diatom genomes sequence PSI-BLAST query/profile Sulfotransferase homologs Diatom Sulfotransferases per genome Phaeodactylum tricornutum 82 (37 secreted) Thalassiosira pseudonana 110 (33 secreted) Phytophthora infestans (oomycetes) 4 Emiliania huxleyi (haptophyte) 122 Ectocarpus siliculosus (phaeophyte/brown alga) 69 Homo sapiens (animal) 59 Arabidopsis thaliana (plant) 24 Neurospora crassa (fungi) 2 Sulfotransferases mainly evolve by lineage-specific expansion Emiliania huxleyi Ehux1000010394 Ectocarpus siliculosus 299471268 Homo sapiens 55749667 Emiliania huxleyi Ehux1000022409 Diatom clade Homo sapiens 54792094 Emiliania huxleyi Ehux1000031183Chromist Homo sapiens 45505173 ThalassiosiraPhaeodactylum pseudonana tricornutum 220969731 217406900ChromistEmiliania Chromist Phaeodactylum tricornutum Diatom217407079Chromist clade Chromist Thalassiosira pseudonana 220967944 Animal Emiliania huxleyi Ehux1000020673Ectocarpus siliculosus 299471476 Chromist Ectocarpus siliculosusHomo sapiens 299473034 23943787 Thalassiosira pseudonana 220974767 Plant EctocarpusEmiliania siliculosushuxleyi Ehux1000002876 298710750 Thalassiosira pseudonanaAnimal 220974286Emiliania huxleyi Ehux1000016421 Emiliania huxleyi Ehux1000024177Emiliania huxleyi Ehux1000005983 0.5 Homo sapiens 74024919 HomoEmiliania sapiens 4507665 huxleyi Ehux1000012711 Homo sapiens 56699463 Ectocarpus siliculosus 299116063 PhaeodactylumThalassiosiraEmiliania tricornutumpseudonana huxleyi 219109876 220974138 Ehux1000013493 Thalassiosira pseudonana 220974537 Thalassiosira pseudonana 220971944 Chromist NeurosporaEctocarpusEmiliania crassa siliculosus 85088847 huxleyi 299116758 Ehux1000003165 Stramenopile Homo sapiens 52694755 Arabidopsis thaliana 42571039 Homo sapiens 4506505 Emiliania huxleyi Ehux1000020299Chromist Emiliania huxleyi Ehux1000017417 Emiliania huxleyi Ehux1000010375 EctocarpusEctocarpus siliculosus siliculosus298710159 299116745 Emiliania huxleyi Ehux1000024153 NeurosporaPhaeodactylumThalassiosira crassa tricornutum 85083976 pseudonana 217405251 220968766 Phaeodactylum tricornutum 219128536 Thalassiosira pseudonana 220972060 Thalassiosira pseudonana 220975478 Phaeodactylum tricornutum 219115061 Thalassiosira pseudonana 209586349 Arabidopsis thaliana 22330856 Ectocarpus siliculosus 299471591 Chromist Emiliania huxleyi Ehux1000030143 Emiliania huxleyi Ehux1000016142 Diatom cladeAnimal EctocarpusEctocarpus Emilianiasiliculosus siliculosus huxleyi 298711123 299473487 Ehux1000002602 Chromist Chromist Chromist Several sequences EctocarpusEmilianiaThalassiosira siliculosushuxleyi Ehux1000007155pseudonana 299470341 220971815 Thalassiosira pseudonana 220975282 Arabidopsis thaliana 22329158 Animal Emiliania huxleyi Ehux1000028171 from a single ChromistArabidopsisArabidopsis thaliana thaliana 79556423 42565806 HomoEmiliania sapiensEmiliania Arabidopsis6912420huxleyi Ehux1000028623huxleyi thaliana Ehux1000021309 186478254 EmilianiaEmiliania huxleyi Ehux1000023385huxleyi Ehux1000002133 Homo sapiensDiatom 5032219 lineage group Chromist ChromistEmiliania together in a Chromist Animal Diatom clade Ectocarpus siliculosus 298714189 Chromist phylogenetic tree Diatom cladeEmiliania Diatom clades ThalassiosiraPhaeodactylum pseudonana tricornutum 220969017 219112905 Chromist clades (Brown algae, haptophytes, diatoms) Suggestive of niche-specific adaptations Several diatom sulfotransferases have signal peptides These sulfotransferases are likely to be secreted into the golgi, where they might modify secreted proteins and carbohydrates. This suggests that the diatom sulfotransferases occupy a unique niche particular to the lifestyle of these species Sulfotransferases Sulfotransferases catalyze the transfer reaction of the sulfate group from the 3’-phosphoadenosine 5’- phosphosulfate (PAPS) to an acceptor group of numerous substrates. Synthesis of PAPS itself requires two ATP molecules: Why this energy expenditure during Phosphate starvation? Sulfate ATP: Sulfurylase Adenylyl sulfate ATP PPi PAPS ATP: adenylylsulfate phosphotranferase ATP ADP Changes in % sulfate and sugar content of extracellular polymers as a function of P status in Phaeodactylum tricornutum 10 80 % Sulfate % Mannose 8 60 6 40 4 % SULFATE % 20 MANNOSECONTENT 2 0 0 HB P-replete HB P-limited HA P-replete HA P-limited HW P-replete HW P-limited TREATMENTS Adapted from Abdullahi et al. 2006 Fe2+ Chelating ability of sulfated Polysaccharides in brown algae CONCENTRATION (mg/ml) Costa et al. 2010) Rapid Creek Pactola Lake Sundareshwar et al.2011 GRL Sundareshwar et al.2011 GRL Fe – Didymo mats Sundareshwar et al.2011 GRL P - Fe – Didymo mats Sundareshwar et al.2011 GRL SEM – D. geminata mat SEM – D. geminata mat Washed Washed – Spiked with Fe & P Sundareshwar et al.2011 GRL Flume Study Larned et al. 2011 4000 Live 3500 Killed 3000 control 2500 2000 1500 1000 % above killed above % 500 0 2+ 2- 2- Fe S SO4 IRON Total Protein Sundareshwar et al.2011 GRL Fe2+ 3- PO4 FeS South Boulder Creek, CO Feb 2010 Confluence of Copper and East rivers, Gothic CO Sept 2009 Image courtesy - Brad Taylor Aerobic zone Biological Throughflow FeP uptake Photosynthates Anaerobic FeP FeS + P zone Biomass & Mat Thickness Mat & Biomass Surface water Sulfate 2- Nutrient Retention & Internal recycling reduction S + CO2 Time Increasing Redox potential Stratification Sundareshwar et al.2011 GRL AMBIENT WATER m) μ ENRICHED WATER Mean stalk length ( length stalk Mean Frequency of Dividing Cells (%) Adapted from Kilroy and Bothwell 2011 Fe + N 03-08-12 03-16-12 New Plant New plant introduced in each jar on 03-14-2012 Fe + P 03-08-12 Take Home Didymo stalks appear to be important in phosphorus acquisition Likely mechanism involves change in the composition of the stalks Increasing sulfation leading to greater negative charge Facilitating cation adsorption Subsequent concentration of phosphorus on to stalks Facilitating redox driven pulsing of phosphorus Sulfotransferases Sulfotransferases catalyze the transfer reaction of the sulfate group from the 3’-phosphoadenosine 5’- phosphosulfate (PAPS) to an acceptor group of numerous substrates. .
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