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Home , Emiliania huxleyi, Thalassiosira pseudonana

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 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) pseudonana 110 (33 secreted) Phytophthora infestans (oomycetes) 4 () 122 Ectocarpus siliculosus (phaeophyte/brown alga) 69 Homo sapiens (animal) 59 Arabidopsis thaliana (plant) 24 Neurospora crassa (fungi) 2 Several sequences phylogenetic tree lineage grouplineage from a single single from a together in a together in Sulfotransferases Chromist Diatom clades

S 220974767 pseudonana Thalassiosira

Thalassiosira pseudonana 220969731 pseudonana Thalassiosira

clades clades Thalassiosira pseudonana 209586349 pseudonana Thalassiosira Thalassiosira pseudonana 220967944 pseudonana Thalassiosira

uggestive nicheof

Emiliania huxleyi Ehux1000020299 huxleyi Emiliania

Emiliania huxleyi Ehux1000024153 huxleyi Emiliania

Phaeodactylum tricornutum 217407079 tricornutum Phaeodactylum

Phaeodactylum tricornutum 217406900 tricornutum Phaeodactylum

Emiliania huxleyi Ehux1000010375 huxleyi Emiliania

Thalassiosira pseudonana 220972060 pseudonana Thalassiosira Arabidopsis thaliana 42571039 thaliana Arabidopsis Ectocarpus siliculosus 299116063 siliculosus Ectocarpus

Diatom clade Stramenopile

(Brown algae, Ectocarpus siliculosus 298714189

Chromist

Chromist mainly evolveby lineage - Chromist Chromist

Chromist

Emiliania huxleyi Ehux1000031183 huxleyi Emiliania

Animal Ehux1000022409 huxleyi Emiliania

Diatom clade Diatom

Thalassiosira pseudonana 220969017 299471268 siliculosus Ectocarpus

Animal 45505173 sapiens Homo

Chromist Chromist Phaeodactylum tricornutum 219112905 Ehux1000010394 huxleyi Emiliania

Emiliania Chromist Diatom clade 55749667 sapiens Homo

Diatom cladeChromist 54792094 sapiens Homo

Chromist Emiliania

clade Diatom Emiliania Chromist 0.5 - , )

specific adaptations Animal Plant Chromist Animal Homo sapiens 74024919 ThalassiosiraChromist pseudonana 220974286

EmilianiaEctocarpusEmiliania huxleyi huxleyisiliculosus Ehux1000024177 Ehux1000020673 299473034

Emiliania huxleyi Ehux1000023385 huxleyi Emiliania Chromist

Homo sapiens 6912420 sapiens Homo Animal

Homo sapiens 5032219 sapiens Homo

Emiliania huxleyi Ehux1000002133 huxleyi Emiliania Emiliania huxleyi Ehux1000028623 huxleyi Emiliania Homo sapiens 23943787 EctocarpusEctocarpus siliculosus siliculosus 298710750 299471476

PhaeodactylumEmilianiaEmiliania tricornutumhuxleyi huxleyi Ehux1000005983 Ehux1000002876219109876

Emiliania huxleyi Ehux1000021309 huxleyi Emiliania

Ectocarpus siliculosus 299470341 siliculosus Ectocarpus Diatom Thalassiosira pseudonana 220974138

Emiliania huxleyi Ehux1000028171 huxleyi Emiliania

Chromist

Arabidopsis thaliana 186478254 thaliana Arabidopsis Ectocarpus siliculosus 298710159

Ectocarpus siliculosus 298711123 siliculosus Ectocarpus Emiliania huxleyi Ehux1000016421 Emiliania huxleyi Ehux1000007155 huxleyi Emiliania Neurospora crassa 85083976

Ectocarpus siliculosus 299473487 siliculosus Ectocarpus Neurospora crassa 85088847

Phaeodactylum tricornutum 217405251

Chromist Thalassiosira pseudonana 220974537

Thalassiosira pseudonana 220975282 pseudonana Thalassiosira HomoHomo sapiens sapiens 56699463 4507665

Chromist

Arabidopsis thaliana 79556423 thaliana Arabidopsis

Thalassiosira pseudonana 220971815 pseudonana Thalassiosira Arabidopsis thaliana 22329158 thaliana Arabidopsis Phaeodactylumtricornutum 219115061

Thalassiosira pseudonana220975478

EctocarpusThalassiosira siliculosus pseudonana 299116758 220971944

Emiliania huxleyi Ehux1000030143 huxleyi Emiliania 22330856 thaliana Arabidopsis Emiliania huxleyi Ehux1000013493 Ectocarpus siliculosus 299471591 siliculosus Ectocarpus Arabidopsis thaliana 42565806 thaliana Arabidopsis Phaeodactylum tricornutum 219128536 Emiliania huxleyi Ehux1000017417

Emiliania huxleyi Ehux1000016142 huxleyi Emiliania HomoHomo sapiens sapiens 4506505 52694755 Emiliania huxleyi Ehux1000012711

Thalassiosira pseudonana 220968766Ectocarpus siliculosus 299116745

Emiliania huxleyi Ehux1000003165 Emiliania huxleyi Ehux1000002602 huxleyi Emiliania specific expansion

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.