Central and storage carbon metabolism of the brown alga Ectocarpus siliculosus : insights into the origin and evolution of storage carbohydrates in Eukaryotes

The enzymes converting triose-phosphate into F6P are well conserved in E. siliculosus.

“The enzymes converting this triose-phosphate into F6P are well conserved in E. siliculosus (Supporting Information Table S1).”

Homologues of the TPI/GAPDH translational fusion are only found in diatoms and Oomycetes.

“Homologues of this translational fusion are only found in diatoms (Armbrust et al., 2004;Bowler et al., 2008) and Oomycetes (Tyler et al., 2006;Haas et al., 2009)”

Ectocarpus contains two standalone proteins highly similar to the Micromonas putative M1Pases (63% sequence identity with MICPUC_47598).

“This assumption is further strengthened by the identification in Ectocarpus of two standalone proteins (Esi0080_0016 and Esi0100_0020) highly similar to the Micromonas putative M1Pases (63% sequence identity with MICPUC_47598).”

Comparison with crystal structures of HAD-like phosphatases confirm that the catalytic machinery is strictly conserved in the putative M1Pases.

“Comparison with crystal structures of HAD-like phosphatases confirm that the catalytic machinery (Ridder & Dijkstra, 1999) is strictly conserved in the putative M1Pases (data not shown).”

The M1PDH sequences of E. tenella and of the Micromonas species are nested within the brown algal clade.

“In contrast, the M1PDH sequences of E. tenella and of the Micromonas species are nested within the brown algal clade.”

These sucrose-metabolism enzymes are also absent in diatoms and Oomycetes, with the exception of the GH32 family of invertases present in Phytophthora species.

“These enzymes are also absent in diatoms and Oomycetes, with the exception of the GH32 family of invertases present in Phytophthora species.”

E. siliculosus possesses a gene, Esi0139_0025, which is closely related to cyanobacterial fructokinases.

“Instead, this seaweed possesses a gene, Esi0139_0025, which is closely related to cyanobacterial fructokinases.”

Gene Esi0187_0027 encodes a modular protein encompassing a TPI fused to a GAPDH.

“Interestingly, the gene Esi0187_0027 encodes a modular protein encompassing a triose-phosphate isomerase (TPI) fused to a glyceraldehyde-3phosphate dehydrogenase (GAPDH).”

The putative M1Pase Esi0080_0016 is located next to the M1PDH gene Esi0080_0017.

“In addition the putative M1Pase Esi0080_0016 is located next to the M1PDH gene Esi0080_0017.”

Homologues of the UGP/PGM fusion-protein are only found in the genomes of Oomycetes and of the diatom P. tricornutum.

“Again, homologues of this UGP/PGM fusion-protein are only found in the genomes of Oomycetes and of the diatom P. tricornutum.”

The three members of the GT48 family display significant similarities with plant callose synthases (~35% sequence identity).

“In contrast, the three members of the GT48 family (Esi0033_0138, Esi0193_0029 and Esi0338_0032) display significant similarities with plant callose synthases (~35% sequence identity).”

Esi0430_0005 displays an additional UGP module at the N-terminus.

“Moreover, Esi0430_0005 displays an additional UDP-glucose-pyrophosphorylase (UGP) module at the N-terminus.”

Ectocarpus possesses a complete trehalose pathway.

“In contrast, Ectocarpus possesses a complete trehalose pathway.”

The phylogenetic tree of the GT48 family is congruent with the currently accepted phylogeny of the Eukaryotes, with the β-1,3-glucan synthases from plants, fungi, Apicomplexa and Stramenopiles consistently emerging as distinct clades.

“The phylogenetic tree of the GT48 family (Fig. 4) is congruent with the currently accepted phylogeny of the Eukaryotes (Fig. 1), with the β-1,3-glucan synthases from plants, fungi, Apicomplexa and Stramenopiles consistently emerging as distinct clades.”

The isoenzymes converting triose-phosphate into F6P mainly differ in their localization (cytosol, mitochondrial or plastid matrices).

“Based on bioinformatic predictions of signal peptides (Gschloessl et al., 2008), the corresponding isoenzymes mainly differ in their localization (cytosol, mitochondrial or plastid matrices).”

Ectocarpus contains two cytosolic isoforms of UDP-glucose pyrophosphorylase (UGP, Esi0144_0004 and Esi0430_0005).

“This seaweed contains two cytosolic isoforms of UDP-glucose pyrophosphorylase (UGP, Esi0144_0004 and Esi0430_0005), supporting the assumption that UDP-glucose is the activated sugar needed for the production of laminarin.”

No ortholog of eukaryotic hexokinases was found in E. siliculosus.

“However, no ortholog of eukaryotic hexokinases was found in E. siliculosus.”

Diatoms and Apicomplexa have conserved only the CMI293C-like TPS.

“In contrast, diatoms and Apicomplexa have conserved only this latter type of TPS (Fig. 3a).”

The β-1,3-glucan synthases of Stramenopiles are divided into three groups.

“The β-1,3-glucan synthases of Stramenopiles are further divided into three groups.”

The degradation of laminarin is potentially catalyzed by ten endo-1,3-β-glucanases belonging to three different families and by two exo-1,3-beta-glucanases.

“The degradation of laminarin is potentially catalyzed by ten endo-1,3-β-glucanases belonging to three different families (GH16: 4 genes; GH17: 1 gene; GH81: 5 genes), and by two exo-1,3-beta-glucanases (family GH5).”

Ectocarpus possesses two proteins homologous to KRE6, a GH16 family transglycosylase involved in β-1,6-branching of cell wall β-1,3-glucans in yeasts.

“In addition, Ectocarpus possesses two proteins (Esi0100_0034 and Esi0243_0020) which are homologous to KRE6, a GH16 family transglycosylase involved in β-1,6-branching of cell wall β-1,3-glucans in yeasts (Montijn et al., 1999).”

The M1PDH and putative M1Pase genes from Ectocarpus are closely related to those of Gram positive bacteria.

“These enzyme activities are indeed rather rare among living organisms and here we show that the M1PDH and putative M1Pase genes from Ectocarpus are closely related to those of Gram positive bacteria (Fig. 2).”

• AssumptionRests on an assumption: The conversion of F6P into mannitol involves two enzymatic steps catalyzed by M1PDH and M1Pase.

M1PDH and putative M1Pase genes are absent from red algae, Chlorophytes, mosses and higher plants.

“between M1PDH and the putative M1Pase genomes and are absent from red algae, Chlorophytes, mosses and higher plants.”

Inspection of the genome of C. merolae indicates that this red alga does not contain any sucrose-related gene.

“Inspection of the genome of C. merolae (Matsuzaki et al., 2004) indicates that this red alga does not contain any sucrose-related gene.”

This GT48 module belongs to clade A, the subgroup that we suggest to be responsible for laminarin polymerization.

“This GT48 module belongs to the clade A (Fig. 4), the very subgroup that we suggest to be responsible for laminarin polymerization.”

Genes involved in sucrose metabolism are completely absent from Stramenopiles genomes, as deduced from the lack of sucrose synthase, sucrose-phosphate synthase and of invertase.

“Similarly, genes involved in sucrose metabolism are completely absent from Stramenopiles genomes, as deduced from the lack of sucrose synthase, sucrose-phosphate synthase and of invertase.”

The six TPS/TPP of Ectocarpus are closely related to their orthologs from C. merolae.

“Here we show that the six TPS/TPP of Ectocarpus are closely related to their orthologs from C. merolae (Fig. 3).”

• AssumptionRests on an assumption: Trehalose synthesis requires two enzyme activities: trehalose-phosphate synthase (TPS) and trehalose-phosphate phosphatase (TPP).

The KRE6-like protein PITG_03335 from P. infestans is fused to a GT48 family β-1,3-glucan synthase.

“Remarkably, the KRE6-like protein PITG_03335 from P. infestans (Haas et al., 2009) is fused to a GT48 family β-1,3-glucan synthase.”

With the exception of GDP-mannose pyrophosphorylase, the enzymes involved in the equilibration of the hexose-phosphate pool and in the generation of activated sugars are conserved with other eukaryotes.

“With the exception of GDP-mannose pyrophosphorylase (Michel et al., 2010), the enzymes involved in the equilibration of the hexose-phosphate pool and in the generation of activated sugars are conserved with other eukaryotes.”

In phylogenetic analyses, Stramenopile M1PDH and putative M1Pase genes cluster with their orthologues in Micromonas (Prasinophytes).

“In the phylogenetic analyses of M1PDH and putative M1PAses, the Stramenopile genes cluster with their orthologues in Micromonas (Prasinophytes), suggesting that these microalgae feature a mannitol metabolism of brown algal origin.”

A systematic search for all these enzymes in Ectocarpus did not retrieve any corresponding gene.

“A systematic search for all these enzymes in Ectocarpus did not retrieve any corresponding gene.”

These numerous laminarinases have homologues in bacteria, fungi and plants, underlining the complexity of laminarin metabolism in brown algae.

“These numerous laminarinases have homologues in bacteria (family GH16), fungi (families GH5 and GH81) and plants (family GH17), underlining the complexity of laminarin metabolism in brown algae.”

The metabolism of β-1,3-glucans involves ancient eukaryotic enzymes.

“Here we demonstrate that the metabolism of β-1,3-glucans involves ancient eukaryotic enzymes.”

Stramenopiles' storage compounds consist of laminarin, a β-1,3-glucan.

“Instead, their storage compounds consist of laminarin, a β-1,3-glucan.”

Oomycetes and Laminariales produce both storage and cell wall β-1,3-glucans.

“Interestingly, such an evolution occurred independently in fungi and in plants, as well as within the Stramenopiles, with Oomycetes and Laminariales producing both storage and cell wall β-1,3-glucans (Parker & Huber, 1965;Bartnicki-Garcia, 1968).”

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β-1,3-glucan synthases from brown algae and other Stramenopiles belong to the GT48 family.

“The β-1,3-glucan synthases from brown algae and other Stramenopiles belong to the GT48 family, a family that is conserved in most eukaryotic phyla, but which is absent from Bacteria and Archaea.”

Other genes of actinobacterial origin in Ectocarpus are not present in Prasinophytes.

“and (iii), the other genes of actinobacterial origin in Ectocarpus are not present in Prasinophytes (Michel et al., 2010), suggesting that there was not a direct HGT from Actinobacteria to Prasinophytes.”

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The phylogenetic tree of the GT48 family is congruent with the currently accepted phylogeny of Eukaryotes.

“The phylogenetic tree of the GT48 family is congruent with the currently accepted phylogeny of Eukaryotes (Fig. 4).”

The conservation between fungi (Unikonts) and Stramenopiles (Bikonts) of KRE6-like proteins (GH16) and some laminarinases (GH5 and GH81) is consistent with the ancestral character of laminarin metabolism.

“The conservation between fungi (Unikonts) and Stramenopiles (Bikonts) of KRE6-like proteins (GH16) and some laminarinases (GH5 and GH81) is also consistent with the ancestral character of laminarin metabolism.”

The indirect debranching enzymes from Apicomplexa have homologues in animals and fungi, but not in Archaeplastida.

“The indirect debranching enzymes from Apicomplexa have homologues in animals and fungi, but not in Archaeplastida, indicating that the aveolate host cell contained its own pathway for glycogen synthesis (Coppin et al., 2005).”

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This would be a rare example of functional clustering in Ectocarpus.

“This would be a rare example of functional clustering in Ectocarpus (Cock et al., 2010).”

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TPS are only present as fusion-proteins in Dictyostelium discoideum, insects, red algae, green algae, plants, Alveolates and Stramenopiles.

“In contrast, TPS are only present as fusion-proteins in Dictyostelium discoideum (Amoebozoa), insects, red algae, green algae, plants, Alveolates and Stramenopiles.”

These eukaryotic phyla acquired TPS from ancestral red algal endosymbiont(s).

“and Alveolates, indicating that these eukaryotic phyla acquired TPS from ancestral red algal endosymbiont(s).”

The TPI/GAPDH bifunctional enzyme is characteristic of Stramenopiles.

“suggesting that this bifunctional enzyme is characteristic of Stramenopiles.”

Phylogenetic analyses suggest that bacterial M1PDH genes were acquired independently by fungi and brown algae.

“Phylogenetic analyses suggest that bacterial M1PDH genes were acquired independently by fungi and brown algae (Fig. 2a).”

Brown algae apparently are an exception to the trend that broad specificity hexokinases are typical of multicellular eukaryotes, whereas sugar-specific kinases are distinctive of bacteria and unicellular eukaryotes.

“Thus, brown algae apparently are an exception to the trend that broad specificity hexokinases are typical of multicellular eukaryotes, whereas sugar-specific kinases are distinctive of bacteria and unicellular eukaryotes (Cardenas et al., 1998).”

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Mannitol is synthesized in two steps: F6P is reduced by M1PDH into mannitol-1P, which is then converted into mannitol by M1Pase.

“Mannitol is synthesized in two steps: F6P is reduced by mannitol-1phosphate 5-dehydrogenase (M1PDH) into mannitol-1P, which is then converted into mannitol by mannitol-1-phosphatase (M1Pase).”

Recycling of mannitol is probably performed by Esi0135_0010, which is similar to bacterial and fungal M2DH.

“Recycling of mannitol is probably performed by Esi0135_0010, which is similar to bacterial and fungal M2DH.”

Laminarin oligosaccharides would be further hydrolyzed by β-glucosidases of the GH1 or GH3 families.

“Laminarin oligosaccharides would be further hydrolyzed by β-glucosidases of the GH1 (Esi0061_0010, Esi0176_0045 and Esi0212_0019) or GH3 families (Esi0010_0226).”

The presence of trehalose was never reported in brown algae before this study.

“To the best of our knowledge, the presence of trehalose was never reported in brown F o r P e e r R e v i e w 17 algae before this study, even in recent reviews (Elbein et al., 2003;Iturriaga et al., 2009).”

Red algae probably acquired sucrose metabolism during primary endosymbiosis as well, even though these photosynthetic organisms are not currently known to produce sucrose.

“Consequently, red algae probably acquired sucrose metabolism during primary endosymbiosis as well, even though these photosynthetic organisms are not currently known to produce sucrose (Kremer, 1980).”

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After the divergence of brown algae from diatoms and Oomycetes, M1PDH and M1Pase were imported into brown algae by a horizontal gene transfer involving an ancestral Gram positive bacterium related to extant Actinobacteria.

“Based on this close phylogenetic relationship, we propose that, after the divergence of brown algae from diatoms and Oomycetes, these two enzymes were imported into brown algae by a horizontal gene transfer involving an ancestral Gram positive bacterium related to extant Actinobacteria.”

• AssumptionRests on an assumption: Brown algae synthesize mannitol as an additional carbon storage sugar.
• AssumptionRests on an assumption: The conversion of F6P into mannitol involves two enzymatic steps catalyzed by M1PDH and M1Pase.
• AssumptionRests on an assumption: The enzyme activities for mannitol synthesis are rather rare among living organisms.

In brown algae, central and storage carbon metabolism is profoundly different from what is known for fungi, animals and plants.

“In brown algae, this metabolism is profoundly different from what is known for fungi, animals and plants, a uniqueness which is further reinforced in the phylogenomic reconstruction of the metabolic routes for the biosynthesis of cell wall polysaccharides (Michel et al., 2010).”

These two proteins represent good candidates for the synthesis of β-1,6-linked branches of laminarin.

“Therefore, these two proteins represent good candidates for the synthesis of β-1,6-linked branches of laminarin.”

In brown algae, F6P can be also directly transformed into a soluble storage compound (mannitol), without prior conversion into an activated sugar.

“In brown algae, however, F6P can be also directly transformed into a soluble storage compound (mannitol), without prior conversion into an activated sugar (Fig. 5).”

The actinobacterium also contributed to the enzyme machinery that synthesizes alginate and hemicelluloses, two major cell wall polysaccharides absent from diatoms and Oomycetes.

“The actinobacterium would also have contributed to the enzyme machinery that synthesizes alginate and hemicelluloses, two major cell wall polysaccharides which are absent from diatoms and Oomycetes.”

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These key sugars are then used by specific enzymes to generate two unique storage compounds, mannitol and laminarin.

“However, these key sugars are then used by specific enzymes to generate two unique storage compounds, mannitol and laminarin.”

The assimilation of the red algal pathway by the host was probably facilitated by the fact that this pathway already consisted of a single bifunctional enzyme, with both TPP and TPS activities, in ancestral red algae.

“The assimilation of the red algal pathway by the host was probably facilitated by the fact that this pathway already consisted of a single bifunctional enzyme, with both TPP and TPS activities, in ancestral red algae (Fig. 5).”

• AssumptionRests on an assumption: Trehalose synthesis requires two enzyme activities: trehalose-phosphate synthase (TPS) and trehalose-phosphate phosphatase (TPP).

Fructose-6-phosphate plays a central role in these pathways.

“Fructose-6phosphate plays a central role in these pathways.”

The bacterial HGT was probably instrumental in the emergence of complex multicellularity in brown algae, by providing extracellular matrix polysaccharides and mannitol for long-distance translocation of photoassimilates.

“Therefore, this bacterial HGT was probably instrumental in the emergence of complex multicellularity in brown algae, by providing two essential elements in this evolutionary process: (i) extracellular matrix polysaccharides for the construction of multicellular tissues and organs, (ii) and mannitol for the long distance translocation of photoassimilates (Parker & Huber, 1965).”

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• AssumptionRests on an assumption: Brown algae synthesize mannitol as an additional carbon storage sugar.

This hypothesis is strengthened by the conservation of KRE6-like proteins in diatoms and Oomycetes.

“This hypothesis is strengthened by the conservation of KRE6-like proteins in diatoms and Oomycetes.”

Micromonas (Prasinophytes) feature a mannitol metabolism of brown algal origin.

“In the phylogenetic analyses of M1PDH and putative M1PAses, the Stramenopile genes cluster with their orthologues in Micromonas (Prasinophytes), suggesting that these microalgae feature a mannitol metabolism of brown algal origin.”

The HGT event extended beyond the acquisition of mannitol metabolism.

“As reported in more detail in the second part of this study (Michel et al., 2010), this HGT event extended beyond the acquisition of mannitol metabolism.”

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The interpretation of Moustafa and coworkers is somewhat weakened from the lack of genomic data from archetypal red algae, which may also possess many of the proposed green algal genes.

“Therefore, the interpretation of Moustafa and coworkers is somewhat weakened from the lack of genomic data from archetypal red algae, which may also possess many of the proposed”

It is very likely that the red alga that gave birth to the phaeoplasts of extant Stramenopiles had already lost the cyanobacterial sucrose-metabolism when the secondary endosymbiosis took place.

“Therefore, it is very likely that the red alga that gave birth to the phaeoplasts of extant Stramenopiles (Reyes-Prieto et al., 2007) had already lost the cyanobacterial sucrosemetabolism when the secondary endosymbiosis took place.”

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Stramenopiles and Alveolates are rather closely related lineages.

“In comparison to the other major eukaryotic groups, Stramenopiles and Alveolates are rather closely related lineages (Baldauf, 2008).”

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Compared to the other eukaryotic phyla, Stramenopiles feature very distinctive traits in their storage carbon metabolism.

“In conclusion, compared to the other eukaryotic phyla, Stramenopiles feature very distinctive traits in their storage carbon metabolism.”

The success of the acquisition of starch metabolism in the Archaeplastida following plastid primary endosymbiosis was probably due to compatibility between biosynthetic pathways in the eukaryotic host cell and in its cyanobiont.

“The success of the acquisition of starch metabolism in the Archaeplastida following plastid primary endosymbiosis was probably due to compatibility between biosynthetic pathways in the eukaryotic host cell and in its cyanobiont.”

Laminarin is an ancestral metabolite in Stramenopiles.

“This finding indicates that β-1,3-glucans were present in the last common ancestor of eukaryotes and that laminarin is an ancestral metabolite in Stramenopiles.”

Following the secondary endosymbiosis, the ancestral host-cell glycogen pathway evolved into a genuine starch metabolism through the transfer of red algal starch-related genes.

“Phylogenetic analyses of other key enzymes for starch synthesis demonstrate that, following the secondary endosymbiosis, the ancestral host-cell glycogen pathway evolved into a genuine starch metabolism through the transfer of red algal starch-related genes (Coppin et al., 2005).”

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The starch biosynthetic pathway characteristic of Archaeplastida results from the merging of the glycogen metabolism of the eukaryotic host cell with the starch metabolism of the cyanobacterial endosymbiont.

“From the seminal work of Steven Ball and colleagues on the origin of starch metabolism, it is now well recognized that this biosynthetic pathway, characteristic of Archaeplastida, results from the merging of the glycogen metabolism of the eukaryotic host cell with the starch metabolism of the cyanobacterial endosymbiont (Ball & Morell, 2003;Deschamps et al., 2008;Plancke et al., 2008).”

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β-1,3-glucans are the archetypal storage polysaccharide in Eukaryotes.

“Therefore, we propose that β-1,3-glucans are the archetypal storage polysaccharide in Eukaryotes (Fig. 6).”

Euglenophytes (Excavata) and Haptophytes, two lineages independent from Stramenopiles, also use β-1,3-glucans as carbon storage.

“Interestingly, Euglenophytes (Excavata) and Haptophytes, two lineages independent from Stramenopiles (Fig. 1), also use β-1,3-glucans as carbon storage (Kiss et al., 1988;Andersen, 2004).”

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Intracellular β-1,3-glucans were the ancestral forms of these carbohydrates.

“It is likely that intracellular β-1,3-glucans were the ancestral forms of these carbohydrates and that they subsequently evolved to be secreted as extracellular polysaccharides as complex multicellularity emerged.”

The alveolate host cell contained its own pathway for glycogen synthesis.

“The indirect debranching enzymes from Apicomplexa have homologues in animals and fungi, but not in Archaeplastida, indicating that the aveolate host cell contained its own pathway for glycogen synthesis (Coppin et al., 2005).”

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β-1,3-glucans were present in the last common ancestor of eukaryotes.

“This finding indicates that β-1,3-glucans were present in the last common ancestor of eukaryotes and that laminarin is an ancestral metabolite in Stramenopiles.”

There was not a direct HGT from Actinobacteria to Prasinophytes.

“and (iii), the other genes of actinobacterial origin in Ectocarpus are not present in Prasinophytes (Michel et al., 2010), suggesting that there was not a direct HGT from Actinobacteria to Prasinophytes.”

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Intracellular β-1,3-glucans subsequently evolved to be secreted as extracellular polysaccharides as complex multicellularity emerged.

“It is likely that intracellular β-1,3-glucans were the ancestral forms of these carbohydrates and that they subsequently evolved to be secreted as extracellular polysaccharides as complex multicellularity emerged.”

The usual fate of storage polysaccharides in bacterial parasites and obligatory symbionts is loss.

“This fate contrasts with the usual loss of storage polysaccharides by bacterial parasites and obligatory symbionts (Henrissat et al., 2002;Gil et al., 2004).”

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Orthologues of M1PDH and putative M1Pase genes are present in brown algal EST libraries.

“In contrast, orthologues of these genes are present in brown algal EST libraries (Roeder et al., 2005;Wong et al., 2007;Pearson et al., 2009);”

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The evolution of β-1,3-glucan secretion occurred independently in fungi, in plants, and within the Stramenopiles.

“Interestingly, such an evolution occurred independently in fungi and in plants, as well as within the Stramenopiles, with Oomycetes and Laminariales producing both storage and cell wall β-1,3-glucans (Parker & Huber, 1965;Bartnicki-Garcia, 1968).”

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The limited number of transferred genes needed for the metabolic transformation from glycogen to starch was also a favorable factor.

“The limited number of transferred genes needed for this metabolic transformation was also a favorable factor (Deschamps et al., 2008).”

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The starch metabolism from the red algal endosymbiont was not retained in Stramenopiles.

“The starch metabolism from the red algal endosymbiont was not retained in Stramenopiles”

• AssumptionRests on an assumption: All the genes required for the complete pathway of glycogen metabolism in heterotrophic Eukaryotes are maintained in red algae.

This metabolic incompatibility resulted in a rapid loss of the starch metabolism of the engulfed red alga.

“Based on the reasoning developed by Ball and coworkers for Archaeplastida, and as observed for obligatory symbionts (Henrissat et al., 2002;Gil et al., 2004), this metabolic incompatibility resulted in a rapid loss of the starch metabolism of the engulfed red alga.”

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Starch metabolism involves a minimal set of ten different enzymes in Rhodophyceae.

“Starch metabolism is a complex process, involving a minimal set of ten different enzymes in Rhodophyceae (Deschamps et al., 2008).”

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The starch pathway of Alveolates is a hybrid metabolism.

“As observed in the Archaeplastida, the starch pathway of Alveolates is a hybrid metabolism.”

The mannitol-related genes in Micromonas were acquired relatively recently from a brown alga by these Prasinophytes.

“Altogether these findings indicate that the mannitol-related genes in Micromonas were acquired relatively recently from a brown alga by these Prasinophytes.”

The transition from glycogen to starch metabolism was due to the transfer of a small number of cyanobacterial genes, namely isoamylase (GH13), granule bound starch synthase I (GBSSI, GT5) and α-(1,4)glucanotransferase (GH77), to the host nuclear genome.

“The transition from glycogen to starch metabolism was due to the transfer of a small number of cyanobacterial genes, namely isoamylase (GH13), granule bound starch synthase I (GBSSI, GT5) and α-(1,4)glucanotransferase (GH77), to the host nuclear genome (Deschamps et al., 2008).”

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Alveolates such as Dinoflagellates and Apicomplexa accumulate starch in their cytoplasm.

“In spite of their phylogenetic relatedness with Stramenopiles, Alveolates such as Dinoflagellates and Apicomplexa accumulate starch in their cytoplasm (Coppin et al., 2005).”

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The occurrence of two independent secondary endosymbiotic events contradicts the Chromalveolate hypothesis.

“The occurrence of two independent, secondary endosymbiotic events contradicts the Chromalveolate hypothesis(Cavalier-Smith, 1999).”

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In brown algae only, a significant HGT happened with an actinobacterium, leading to the de novo acquisition of an additional pathway for carbon storage, based on mannitol.

“Finally, in brown algae only, a significant HGT happened with an actinobacterium, leading to the de novo acquisition of an additional pathway for carbon storage, based on mannitol.”

• AssumptionRests on an assumption: Brown algae synthesize mannitol as an additional carbon storage sugar.

The most parsimonious scenario is that Eukaryotes acquired glycogen metabolism from the alphaproteobacterial progenitor of mitochondria.

“The most parsimonious scenario is that Eukaryotes acquired glycogen metabolism from the alphaproteobacterial progenitor of mitochondria (Fig. 6).”

In the ancestors of extant Stramenopiles, the bacterial glycogen metabolism was lost.

“In the ancestors of extant Stramenopiles, the bacterial glycogen metabolism was lost (Fig. 6).”

A variety of other major speciation events further contributed to the striking metabolic uniqueness of the brown algal lineage.

“From a similar phylogenomic analysis of the enzymes involved in cell wall polysaccharides synthesis, we show that a variety of other major speciation events further contributed to the striking metabolic uniqueness of this lineage (Michel et al., 2010).”

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In most eukaryote lineages, glycogen then supplanted β-1,3-glucan as the form of carbon storage.

“In most of them, glycogen then supplanted β-1,3 glucan as the form of carbon storage.”

It is very unlikely that two lineages with the same original genetic background would have evolved two so strikingly different carbon storage metabolisms.

“It is very unlikely that two lineages with the same original genetic background, that is, genomes from the same ancestral host and rhodobiont cells would have evolved two so strikingly different carbon storage metabolisms.”

Brown algae have inherited an ancestral trehalose metabolism from their red algal endosymbiont.

“Considering also that they have inherited an ancestral trehalose metabolism from their red algal endosymbiont, brown algae have evolved a very unique central and storage carbon metabolism.”

• AssumptionRests on an assumption: Trehalose synthesis requires two enzyme activities: trehalose-phosphate synthase (TPS) and trehalose-phosphate phosphatase (TPP).

Brown algae have evolved a very unique central and storage carbon metabolism.

“Considering also that they have inherited an ancestral trehalose metabolism from their red algal endosymbiont, brown algae have evolved a very unique central and storage carbon metabolism.”

• AssumptionRests on an assumption: Brown algae synthesize mannitol as an additional carbon storage sugar.
• AssumptionRests on an assumption: Trehalose synthesis requires two enzyme activities: trehalose-phosphate synthase (TPS) and trehalose-phosphate phosphatase (TPP).