Steven G Ball

• PhD
• Professor (Full) at University of Lille Nord de France

Haptophytes synthesize unique β-glucans containing more β-1,6-linkages than β-1,3 linkages, as a storage polysaccharide. To understand the mechanism of the synthesis, we investigated the roles of Kre6 (yeast 1,6-β-transglycosylase) homologs, PhTGS, in the haptophyte Pleurochrysis haptonemofera. RNAi of PhTGS repressed β-glucan accumulation and simu...

Most rhodophytes synthesize semi-amylopectin as a storage polysaccharide, whereas some species in the most primitive class (Cyanidiophyceae) make glycogen. To know the roles of isoamylases in semi-amylopectin synthesis, we investigated the effects of isoamylase gene (CMI294C and CMS197C)-deficiencies on semi-amylopectin molecular structure and star...

The order Chlamydiales includes obligate intracellular pathogens capable of infecting mammals, fishes and amoeba. Unlike other intracellular bacteria for which intracellular adaptation led to the loss of glycogen metabolism pathway, all chlamydial families maintained the nucleotide-sugar dependent glycogen metabolism pathway i.e. the GlgC-pathway w...

Eukaryotes most often synthesize storage polysaccharides in the cytosol or vacuoles in the form of either alpha (glycogen/starch)- or beta-glucosidic (chrysolaminarins and paramylon) linked glucan polymers. In both cases, the glucose can be packed either in water-soluble (glycogen and chrysolaminarins) or solid crystalline (starch and paramylon) fo...

All obligate intracellular pathogens or symbionts of eukaryotes lack glycogen metabolism. Most members of the Chlamydiales order are exceptions to this rule as they contain the classical GlgA-GlgC-dependent pathway of glycogen metabolism that relies on the ADP-Glucose substrate. We surveyed the diversity of Chlamydiales and found glycogen metabolis...

Identification and sequence analysis of 180 STs of the GT29 CAZy family Sialic acids are nine-carbon α-keto acids with a carboxylic group found at the outermost positions of lipids and proteins. The biosynthesis of sialylated molecules of crucial relevance for eukaryotic cell life is achieved by the inverting enzymes known as sialyltransferases (ST...

Glaucophyta are members of the Archaeplastida, the founding group of photosynthetic eukaryotes that also includes red algae (Rhodophyta), green algae, and plants (Viridiplantae). Here we present a high-quality assembly, built using long-read sequences, of the ca. 100 Mb nuclear genome of the model glaucophyte Cyanophora paradoxa. We also conducted...

Menaquinone (vitamin K2) shuttles electrons between membrane-bound respiratory complexes under microaerophilic conditions. In photosynthetic eukaryotes and cyanobacteria, phylloquinone (vitamin K1) participates in photosystem I function. Here we elucidate the evolutionary history of vitamin K metabolism in algae and plants. We show that Chlamydiale...

Starch synthases (SSs) are responsible for depositing the majority of glucoses in starch. Structural knowledge on these enzymes that is available from the crystal structures of rice granule bound starch synthase (GBSS) and barley SSI provides incomplete information on substrate binding and active site architecture. Here we report the crystal struct...

The sections in this article are Introduction Synthesis of Bacterial Glycogen Synthesis of Starch in Vascular Plants Starch Synthesis and Breakdown in Leaves and Tubers Control of Starch Biosynthesis in Monocotyledonous Species Starch Synthesis in Green Algae Starch Synthesis in Other Systems Control of Starch Biosynthesis Opportunities fo...

The biosynthesis of sialylated molecules of crucial relevance for eukaryotic cell life is achieved by sialyltransferases (ST) of the CAZy family GT29. These enzymes are widespread in the Deuterostoma lineages and more rarely described in Protostoma, Viridiplantae and various protist lineages raising the question of their presence in the Last eukary...

Biotic interactions underlie life’s diversity and are the lynchpin to understanding its complexity and resilience within an ecological niche. Algal biologists have embraced this paradigm, and studies building on the explosive growth in omics and cell biology methods have facilitated the in-depth analysis of nonmodel organisms and communities from a...

Blastocystis is the most prevalent eukaryotic microbe colonizing the human gut, infecting approximately 1 billion individuals worldwide. Although Blastocystis has been linked to intestinal disorders, its pathogenicity remains controversial because most carriers are asymptomatic. Here, the genome sequence of Blastocystis subtype (ST) 1 is presented...

Supplemental Analyses. (DOCX)

Genome browser screengrab of overlapping genes models in Blastocystis ST4. The 3′ ends of KNB46045 and KNB46046 overlap on scaffold NW_014569526. The presently annotated stop codon for KNB46045 (TGA) is represented by a red box with a dark blue outline. Where polyadenylation starts and creates an alternative stop codon (TAA) is indicated with a tra...

Median read depth of scaffolds greater than 10,000 bps in Blastocystis ST1. Read depth was scaled to give the median value (113) of the scaffold medians a value of 1.00. (DOCX)

Distribution of read depth along the nondisomic scaffold 113. Y-axis corresponds to read depth, x-axis shows scaffold position. Upper bar denotes median read depth for scaffold 113 (213), while lower bar indicates median read depth (113) of all scaffolds over 10,000 bps. (DOCX)

Distribution of read depth along disomic scaffold 102. Y-axis corresponds to read depth, x-axis shows scaffold position. Horizontal bar denotes median read depth for scaffold 102 as well as indicating median read depth (113) of all scaffolds over 10,000 bps. (DOCX)

Telomerase-related genes in Blastocystis STs 1, 4, and 7. (DOCX)

Copy numbers of 60S ribosomal proteins in Blastocystis ST1 and ST7. (DOCX)

Classification of proteases—Blastocystis STs 1, 4, and 7. (XLSX)

General model for meiotic recombination in Blastocystis ST1. Abbreviations: CO, crossover; DSB, double-strand break; NCO, noncrossover. (DOCX)

Distribution of allele frequencies of heterozygous sites across Blastocystis ST1 genomic scaffolds. (DOCX)

GC profile and GC content graphs for Blastocystis ST1, ST4, and ST7. GC profile graphs (A1, B1, and C1 for ST1, ST4, and ST7, respectively) are based on a windowless method. Straight lines denote a region of relatively homogenous GC content. An upward line indicates an abrupt increase in GC content while a downward line indicates an abrupt decrease...

Median sequence identity of matching regions of orthologous proteins from pairs of protozoan pathogens. (DOCX)

Number of different CAZy families found in Blastocystis ST1 and selected stramenopile genomes. (DOCX)

Blastocystis ST1 protein models with matches to a Chlamydomonas reinhardtii flagellar data set. (DOCX)

Secretome for Blastocystis ST1. (XLSX)

Introns in Blastocystis STs 1, 4, and 7. (XLSX)

Sequence logo of signal peptides in 89 Blastocystis ST1 secreted proteins. (DOCX)

40S ribosomal protein S23 and flanking genes in Blastocystis ST1 and ST7. The middle gene corresponds to RPS23. ST1 genes are in blue, ST7 in red. ST1 has 6 copies of RPS23, all of which differ from each other at the nucleotide level. The 3 copies of RPS23 in ST7 are aligned with the corresponding copy in ST1 based on similar flanking genes. Two ST...

α-glucan-related genes in Cafeteria transcriptomes. (DOCX)

Ras superfamily GTPases in Blastocystis STs 1, 4, and 7. (XLS)

Presence of components of the membrane-trafficking machinery in Blastocystis ST1, ST4, and ST7 compared with the last eukaryotic common ancestor (LECA). The numbers within the pie slices indicate the number of isoforms. (DOCX)

Minor spliceosome-specific components in Blastocystis ST1 and ST7. (DOCX)

Telomeric repeats (TTAGGG) in Blastocystis ST1. (DOCX)

Copy numbers of 40S ribosomal proteins in Blastocystis ST1 and ST7. (DOCX)

Carbohydrate active enzymes (CAZymes) present in Blastocystis ST1 and selected stramenopile genomes. Abbreviations: CBM, carbohydrate-binding modules; CE, carbohydrate esterases; GH, glycosyl hydrolases; GT, glycosyl transferases; PL, polysaccharide lyase. (DOCX)

Mitochondrial predicted proteome—Blastocystis ST1. (XLSX)

DNA repair and meiosis-specific and related loci in Blastocystis STs 1, 4, and 7. (XLSX)

Carbohydrate active enzymes—Blastocystis ST1. (XLSX)

Intermediary metabolism—Blastocystis ST1. (XLSX)

Proteins suspected to be involved in cytokinesis—Blastocystis ST1. (XLSX)

Calcium-associated proteins—Blastocystis ST1. (XLSX)

Anaphase promoting complex (APC) subunits—Blastocystis ST1. (XLSX)

Amino acid identities for orthologs. (TXT)

Biotic interactions underlie life's diversity and are the lynchpin to understanding its complexity and resilience within an ecological niche. Algal biologists have embraced this paradigm, and studies building on the explosive growth in omics and cell biology methods have facilitated the in‐depth analysis of nonmodel organisms and communities from a...

Branching enzyme (BE) catalyzes the formation of α-1,6-glucosidic linkages in amylopectin and glycogen. The reaction products are variable depending on the organism sources, and the mechanistic basis for these different outcomes is unclear. Although most cyanobacteria have only one BE isoform belonging to glycoside hydrolase (GH) family 13, Cyanoth...

The plastid originated 1.5 billion years ago through a primary endosymbiosis involving a heterotrophic eukaryote and an ancient cyanobacterium. Phylogenetic and biochemical evidence suggests that the incipient endosymbiont interacted with an obligate intracellular chlamydial pathogen that housed it in an inclusion. This aspect of the ménage-à-trois...

Chlamydiales were recently proposed to have sheltered the future cyanobacterial ancestor of plastids in a common inclusion. The intracellular pathogens are thought to have donated those critical transporters that triggered the efflux of photosynthetic carbon and the consequent onset of symbiosis. Chlamydiales are also suspected to have encoded glyc...

It has been believed that isoamylase (ISA)-type α-glucan debranching enzymes (DBEs) play crucial roles not only in α-glucan degradation but also in the biosynthesis by affecting the structure of glucans, although molecular basis on distinct roles of the individual DBEs has not fully understood. In an attempt to relate the roles of DBEs to their cha...

Chain-length preference of rice isoamylase3 (OsISA3) in debranching amylopectin. Upper panel shows the amount of chains liberated after enzymatic reaction with OsISA3 and amylopectin for 5 (●), 10 (▲), 30 (■), and 60 (♦) min, respectively. Lower panel shows the molar percentage of each liberated chain to the total liberated chains. (TIF)

Chain-length preference of Cyanothece ATCC 51142 isoamylase (CytISA) in debranching amylopectin. Upper panel shows the amount of chains liberated after enzymatic reaction with CytISA and amylopectin for 5 (●), 10 (▲), 30 (■), and 60 (♦) min, respectively. Lower panel shows the molar percentage of each liberated chain to the total liberated chains....

Chain-length preference of Synechococcus elongatus PCC7942 isoamylase1 (ScoISA) in debranching amylopectin. Upper panel shows the amount of chains liberated after enzymatic reaction with ScoISA and amylopectin for 5 (●), 10 (▲), 30 (■), and 60 (♦) min, respectively. Lower panel shows the molar percentage of each liberated chain to the total liberat...

Phylogenetic tree of α-glucan debranching enzymes. DBEs used in this study were shown in the parenthesis. (TIF)

SDS-PAGE of purified DBE preparations used in this study. (TIF)

Chain-length preference of Escherichia coli GlgX (EcoGlgX) in debranching amylopectin. Upper panel shows the amount of chains liberated after enzymatic reaction with EcoGlgX and amylopectin for 5 (●), 10 (▲), 30 (■), and 60 (♦) min, respectively. Lower panel shows the molar percentage of each liberated chain to the total liberated chains. (TIF)

Chain-length distribution of amylopectin and phytoglycogen. Amylopectin from mature endosperm of rice japonica cultivar Nipponbare and phytoglycogen from mature endosperm of rice sugary-1 mutant line EM 914 [14]. (TIF)

Chain-length preference of Pseudomonas amyloderamosa isoamylase (PsaISA) in debranching amylopectin. Upper panel shows the amount of chains liberated after enzymatic reaction with PsaISA and amylopectin for 5 (●), 10 (▲), 30 (■), and 60 (♦) min, respectively. Lower panel shows the molar percentage of each liberated chain to the total liberated chai...

At variance with the starch accumulating plants and most of the glycogen-accumulating cyanobacteria, Cyanobacterium sp. CLg1 synthesizes both glycogen and starch. We now report the selection of a starchless mutant of this cyanobacterium that retains wild-type amounts of glycogen. Unlike other mutants of this type found in plants and cyanobacteria,...

Several groups have independently proposed an active role for Chlamydiales in primary plastid establishment in Archaeplastida (Huang and Gogarten, 2007; Becker et al., 2008; Moustafa et al., 2008). We relied on a combination of biochemical and phylogenetic evidence to erect the MAT (Menage a Trois) hypothesis (Ball et al., 2013; Facchinelli et al.,...

List of siRNAs. DOI: http://dx.doi.org/10.7554/eLife.12552.024

Primers used for cloning purposes. DOI: http://dx.doi.org/10.7554/eLife.12552.023

List of primers used in qRT-PCR and RT-PCR. DOI: http://dx.doi.org/10.7554/eLife.12552.025

Mitochondria and plastids are essential for harnessing energy in eukaryotic cells. They are believed to have formed through primary endosymbioses, in which bacterial symbionts were converted into energy-producing organelles. Primary endosymbiosis is extremely rare: Only one other case is known, in the amoeba Paulinella ( 1 ). This rarity is usually...

A number of recent papers have brought suggestive evidence for an active role of Chlamydiales in the establishment of the plastid. Chlamydiales define a very ancient group of obligate intracellular bacterial pathogens that multiply in vesicles within eukaryotic phagotrophic host cells such as animals, amoebae or other protists, possibly including t...

Several cyanobacterial species, including Cyanothece sp. ATCC 51142, remarkably have four isoforms of α-glucan branching enzymes (BEs). Based on their primary structures, they are classified into glycoside hydrolase (GH) family 13 (BE1, BE2 and BE3) or family 57 (GH57 BE). In the present study, GH13-type BEs from Cyanothece sp. ATCC 51142 (BE1, BE2...

Plastid endosymbiosis defines a process through which a fully evolved cyanobacterial ancestor has transmitted to a eukaryotic phagotroph the hundreds of genes required to perform oxygenic photosynthesis, together with the membrane structures, and cellular compartment associated with this process. In this review, we will summarize the evidence point...

α-1,4-linked glucan chains branched through ’-1,6 glucosidic lineages define the most frequently found storage polysaccharides in living cells. These glucans come in two very distinct forms known as glycogen and starch. The small water-soluble glycogen particles distribute widely in Archaea, Bacteria, and heterotrophic eukaryotes, while semicrystal...

To investigate the functional properties of 10 α-glucan branching enzymes (BEs) from various sources, we determined the chain-length distribution of BE enzymatic products and their phosphorylase-limit dextrins (Φ-LD). All BEs could be classified into either of the three rice BE isozymes: OsBEI, OsBEIIa, or OsBEIIb. Escherichia coli BE (EcoBE) had t...

The starch debranching enzymes isoamylase 1 and 2 (ISA1 and ISA2) are known to exist in a large complex and are involved in the biosynthesis and crystallization of starch. It is suggested that the function of the complex is to remove misplaced branches of growing amylopectin molecules, which would otherwise prevent the association and crystallizati...

Background Starch is the main source of carbon storage in the Archaeplastida. The starch biosynthesis pathway (sbp) emerged from cytosolic glycogen metabolism shortly after plastid endosymbiosis and was redirected to the plastid stroma during the green lineage divergence. The SBP is a complex network of genes, most of which are members of large mul...

Plastid endosymbiosis was selected through the establishment of a biochemical link between the disconnected metabolic networks of the cyanobiont and its eukaryote host. This link is likely to have consisted of the efflux of photosynthetic carbon from the bacterial symbiont to the cytosol of the eukaryote. Storage molecules are suspected to have pla...

Starch, unlike hydrosoluble glycogen particles, aggregates into insoluble, semicrystalline granules. In photosynthetic eukaryotes, the transition to starch accumulation occurred after plastid endosymbiosis from a preexisting cytosolic host glycogen metabolism network. This involved the recruitment of a debranching enzyme of chlamydial pathogen orig...

The endosymbiont hypothesis proposes that photosynthate from the cyanobiont was exported to the cytosol of the eukaryote host and polymerized from ADP-glucose into glycogen. Chlamydia-like pathogens are the second major source of foreign genes in Archaeplastida, suggesting that these obligate intracellular pathogens had a significant role during th...

In this opinion article we propose a scenario detailing how two crucial components have evolved simultaneously to ensure the transition of glycogen to starch in the cytosol of the Archaeplastida last common ancestor: (i) the recruitment of an enzyme from intracellular Chlamydiae pathogens to facilitate crystallization of α-glucan chains; and (ii) t...

A screen was recently developed to study the mobilization of starch in the unicellular green alga Chlamydomonas reinhardtii. This screen relies on starch synthesis accumulation during nitrogen starvation followed by the supply of nitrogen and the switch to darkness. Hence multiple regulatory networks including those of nutrient starvation, cell cyc...

Partial purification of branching enzyme 1 activity from the CAT16 mutant crude extract. The enzymatic defect in the CAT 16 mutant can be observed through the lack of a pink or a red band (enlighted by arrows) on native (a; left panel) and denaturing (a; right panel) starch zymograms respectively. This activity cannot be detected in the first eluti...

Kinetics of starch mobilization in the insertional mutants. The amount of starch measured in the CAT mutant strains is displayed as percentages of the initial content after 4, 8 and 24 h of degradation. The class 1 mutants are presented in a while the class 2 and 3 are shown in b and c respectively. Each bar is mean ±SE of three independent experim...