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Cited by 102Biofuel production and bioconversionAlgal biology and biofuel productionEnzyme Production and Characterization

The Enzymatic Conversion of Major Algal and Cyanobacterial Carbohydrates to Bioethanol

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Al Abdallah, Qusai, Nixon, B. Tracy, Fortwendel, Jarrod R.·2016·Frontiers in Energy Research
DOI 10.3389/fenrg.2016.00036
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Abstract

The production of fuels from biomass is categorized as first-, second- or third-generation depending upon the source of raw materials, either food crops, lignocellulosic material, or algal biomass, respectively. Thus far, the emphasis has been on using food crops creating several environmental problems. To overcome these problems, there is a shift toward bioenergy production from non-food sources. Algae, which store high amounts of carbohydrates, are a potential producer of raw materials for sustainable production of bioethanol. Algae store their carbohydrates in the form of food storage sugars and structural material. In general, algal food storage polysaccharides are composed of glucose subunits, however they vary in the glycosidic bond that links the glucose molecules. In starch-type polysaccharides (starch, floridean starch, and glycogen), the glucose subunits are linked together by α-(1→4) and α-(1→6) glycosidic bonds. Laminarin-type polysaccharides (laminarin, chrysolaminarin, and paramylon) are made of glucose subunits that are linked together by β-(1→3) and β-(1→6) glycosidic bonds. In contrast to food storage polysaccharides, structural polysaccharides vary in composition and glycosidic bond. The industrial production of bioethanol from algae requires efficient hydrolysis and fermentation of different algal sugars. However, the hydrolysis of algal polysaccharides employs more enzymatic mixes in comparison to terrestrial plants. Similarly, algal fermentable sugars display more diversity than plants, and therefore more metabolic pathways are required to produce ethanol from these sugars. In general, the fermentation of glucose, galactose, and glucose isomers is carried out by wild type strains of Saccharomyces cerevisiae and Zymomonas mobilis. In these strains, glucose enters glycolysis, where is it converted to pyruvate through either Embden-Meyerhof-Parnas pathway or Entner-Doudoroff pathway. Other monosaccharides must be converted to fermentable sugars before entering glycolysis. In contrast, microbial wild type strains are not capable of producing ethanol from alginate, and therefore the production of bioethanol from alginate was achieved by using genetically engineered microbial strains, which can simultaneously hydrolyze and ferment alginate to ethanol. In this review, we emphasize the enzymatic hydrolysis processes of different algal polysaccharides. Additionally, we highlight the major metabolic pathways that are employed to ferment different algal monosaccharides to ethanol.

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Written from the paper’s full text.

TL;DR

This review describes the enzymatic hydrolysis of major algal and cyanobacterial carbohydrates and the metabolic pathways used to ferment the resulting sugars to bioethanol. It emphasizes that algal polysaccharides require more diverse enzyme mixtures and fermentation pathways than terrestrial plant biomass, with alginate conversion requiring genetically engineered microbes.

Key findings

  • Algal carbohydrates are structurally diverse: starch-type reserves (starch, floridean starch, glycogen) use α-(1→4) and α-(1→6) bonds; laminarin-type reserves (laminarin, chrysolaminarin, paramylon) use β-(1→3) and β-(1→6) bonds; structural polysaccharides include cellulose, agarose, carrageenan, alginate, ulvan, and fucoidan.
  • Macroalgal biomass production greatly exceeds microalgal production: in 2010, approximately 9 million wet metric tons (WMT) of red macroalgae and 6.75 million WMT of brown macroalgae were harvested, compared with only 6.2 thousand dry metric tons (DMT) from major microalgal species; 93% of cultivated macroalgal biomass came from four genera (Laminaria 65.8%, Undaria 9.8%, Porphyra 12.6%, Gracilaria 4.8%).
  • Reported carbohydrate contents include starch reaching about 50% of dry weight in some species, floridean starch up to 80% of cell volume in Seirospora griffithsiana, laminarin up to 32–35% of dry weight, mannitol about 25% in Laminaria hyperborea, 30% in Laminaria japonica, and 33% in several Sargassum and Turbinaria dry weight, alginate about 30–60% of total sugars, ulvan 8–29% dry weight, and fucoidan 5–20% dry weight.
  • Wild-type Saccharomyces cerevisiae and Zymomonas mobilis ferment glucose, galactose, fructose, and mannose via glycolysis and alcoholic fermentation, but alginate requires engineered strains; an engineered S. cerevisiae fermented up to 83% of brown algae theoretical total sugars, an engineered E. coli fermented 80% of maximum theoretical yield and produced 0.281 weight ethanol/weight dry macroalgae, and a RAGE-engineered strain produced a 330% higher titer than its plasmid-based counterpart after 50 generations.

Methods

  • Design: narrative review of enzymatic hydrolysis and fermentation processes for converting major algal and cyanobacterial carbohydrates to bioethanol.
  • Data or sample: published literature and referenced studies; no new experimental data or primary biological samples were generated.
  • Main analysis: synthesis of polysaccharide structures, hydrolytic enzymes, and microbial metabolic pathways, with tables and figures summarizing algal sources, carbohydrate compositions, and advantages/disadvantages of different algal sugars.

Limitations

  • The paper states that the topic is broad and only fundamental concepts are addressed, with readers referred to complementary reviews.
  • The paper states that several areas are understudied: carrageenan degradation is among the least studied major cell wall carbohydrates; few studies have investigated bioethanol production from floridean starch or laminarin-type polysaccharides; ulvan and fucoidan hydrolysis has been studied less intensively; and the amount of glycogen degradation achieved with only α-amylase and glucoamylase is unknown because synergistic effects and final hydrolysis products were not analyzed.
  • Evident from the text: as a review, it provides no new experimental validation, and industrial feasibility remains constrained by the need for more enzyme mixtures, robust engineered microbes, and pretreatment of rigid structural polysaccharides.

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Integrity signals

Registry

Crossref · 10.3389/fenrg.2016.00036

Cites

Statistics

Nothing to recompute.

Claims the paper makes

0 of 97 cited sources checked · 0 supported · 0 flagged

  • Interpretationreasoning

    Red and brown macroalgae serve as an unexploited potential source for bioethanol production.

    “Although commercial third-generation biofuels are derived from microalgal biomass, seaweeds (specifically red and brown macroalgae) serve as an unexploited potential source for bioethanol production due to two facts.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Commercial third-generation biofuels are derived from microalgal biomass.
  • Premisecitation

    The fresh water requirement for algal growth is significantly lower than plant demands to produce the same volume of biofuel.

    “Finally, the fresh water requirement for algal growth is significantly lower than plant demands to produce the same volume of biofuel.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites John et al. (2011) source

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  • Interpretationreasoning

    Algal biomass is an emerging alternative for the production of biofuels.

    “Therefore, algal biomass is an emerging alternative for the production of biofuels.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Commercial production of second-generation biofuels is limited to countries with large agricultural and forestry lands.
  • Premisenone given

    Algal fermentable sugars display more diversity than plant sugars.

    “Similarly, algal fermentable sugars display more diversity than plants, and therefore more metabolic pathways are required to produce ethanol from these sugars.”
    Quote in the paperNot a substantial claim
  • Premisecitation

    In their marine natural habitats, the productivity of microalgae is very low, not exceeding 10% of that for macroalgae under the same conditions.

    “In their marine natural habitats, the productivity of microalgae is very low, not exceeding 10% of that for macroalgae under the same conditions.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Lüning and Pang, 2003

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  • May combine two claims. 36
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    Premisecitation

    Expansion of biofuel production from food crops has caused environmental impacts including conversion of agricultural land from food crops to biofuel crops and deforestation of hundreds of thousands of acres.

    “Nevertheless, expansion in biofuel production from food crops has drawn attention to several environmental impacts, such as the conversion of agricultural land from producing food crops to producing biofuel crops and the deforestation of hundreds of thousands of acres (Groom et al., 2008;Searchinger et al., 2008;Naik et al., 2010).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Groom et al., 2008;Searchinger et al., 2008;Naik et al., 2010

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    Premisecitation

    Algae grow in aquatic habitats and thereby do not compete with food crops on agricultural land or cause deforestation.

    “Second, algae grow in aquatic habitats and thereby do not compete with food crops on agricultural land, or cause deforestation.”
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    • cites John et al. (2011) source

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    Premisecitation

    In 2010, approximately 9 million and 6.75 million wet metric tons were harvested from red and brown macroalgae, respectively.

    “For example, in 2010, approximately 9 million and 6.75 million wet metric tons (WMT) were harvested from red and brown macroalgae, respectively (Jung et al., 2013).”
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    • cites Jung et al., 2013 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Premisenone given

    Microalgae are the major current source for third-generation biofuels.

    “Currently, microalgae are the major source for third-generation biofuels.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Cultivation of microalgae in open ponds involves lower capital and operating costs but offers low productivity.

    “In contrast, cultivation of microalgae in open ponds involves lower capital and operating costs but offers low productivity.”
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    • cites Chisti, 2016 source

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    Premisecitation

    Microalgal cultures growing in open ponds are exposed to contaminants and affected by seasonal variations.

    “Additionally, microalgal cultures growing in open ponds are exposed to contaminants and affected by seasonal variations (Chisti, 2016).”
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    • cites Chisti, 2016 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisenone given

    Other monosaccharides must be converted to fermentable sugars before entering glycolysis.

    “Other monosaccharides must be converted to fermentable sugars before entering glycolysis.”
    Quote in the paperNot a substantial claim

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    Premisecitation

    Enzymatic hydrolysis produces high amounts of fermentable sugars under mild conditions without producing inhibitory byproducts.

    “In contrast, enzymatic hydrolysis produces high amounts of fermentable sugars under mild conditions without producing inhibitory byproducts (Chen et al., 2013).”
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    • cites Chen et al., 2013 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Premisenone given

    Fermentation of glucose, galactose, and glucose isomers is carried out by wild-type strains of Saccharomyces cerevisiae and Zymomonas mobilis.

    “In general, the fermentation of glucose, galactose, and glucose isomers is carried out by wild-type strains of Saccharomyces cerevisiae and Zymomonas mobilis.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S4 (based).

    Premisenone given

    The enzymatic hydrolysis of algal polysaccharides requires a wider range of enzymatic mixtures compared to plants.

    “The enzymatic hydrolysis of algal polysaccharides requires a wider range of enzymatic mixtures, compared to plants.”
    • Also stated in: § Abstract · plain
      “However, the hydrolysis of algal polysaccharides employs more enzymatic mixes in comparison to terrestrial plants.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisenone given

    Wild-type microbial strains cannot produce ethanol from alginate, whereas genetically engineered microbial strains can simultaneously hydrolyze and ferment alginate to ethanol.

    “In contrast, microbial wild-type strains are not capable of producing ethanol from alginate, and therefore the production of bioethanol from alginate was achieved by using genetically engineered microbial strains, which can simultaneously hydrolyze and ferment alginate to ethanol.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    The photobioreactor system produces high biomass under controlled growth conditions but requires high capital and operating costs.

    “The photobioreactor system, which produces high biomass under controlled growth conditions, requires high capital and operating costs (Pruvost et al., 2016).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Pruvost et al., 2016 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Premisenone given

    In Saccharomyces cerevisiae and Zymomonas mobilis, glucose enters glycolysis and is converted to pyruvate through either the Embden-Meyerhof-Parnas pathway or the Entner-Doudoroff pathway.

    “In these strains, glucose enters glycolysis, where is it converted to pyruvate through either Embden-Meyerhof-Parnas pathway or Entner-Doudoroff pathway.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Algae serve as non-food feedstock that does not compromise food security.

    “First, algae serve as non-food feedstock, which does not compromise our food security.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites John et al. (2011) source

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  • May combine two claims.

    Premisecitation

    Algal biomass can be used to produce bioethanol and biodiesel because algae accumulate high amounts of carbohydrates and lipids.

    “Third, algal biomass can be used to produce two types of biofuel (bioethanol and biodiesel) since they accumulate high amounts of carbohydrates and lipids.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites John et al. (2011) source

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    Premisecitation

    In comparison to terrestrial plants, macroalgae grow faster and produce more biomass per area due to their high photosynthetic efficiency.

    “In comparison to terrestrial plants, macroalgae grow faster and produce more biomass per area due to their high photosynthetic efficiency (Murphy et al., 2013;Yanagisawa et al., 2013).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Murphy et al., 2013;Yanagisawa et al., 2013

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Starch enzymatic hydrolysis is complex and requires the activity of several enzymes, such as α-amylase, isoamylase, pullulanase, β-amylase, and glucoamylase.

    “Starch enzymatic hydrolysis is complex and requires the activity of several enzymes, such as α-amylase, isoamylase, pullulanase, β-amylase, and glucoamylase.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Van Zyl et al., 2012 source

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    Premisecitation

    Neoagarobiose consists of α-(1→3)-linked l-AnGal and d-Gal residues.

    “In contrast, neoagarobiose consists of α-(1→3)-linked l-AnGal and d-Gal residues.”
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    • cites Renn, 1997 source

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    • cites Fu and Kim, 2010

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    • cites Delattre et al., 2011 source

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    Premisecitation

    Fucoidan displays a general backbone consisting predominantly of α-(1→2)-linked sulfated l-fucose units and, in smaller amounts, α-(1→3)- and α-(1→4)-linked sulfated fucose units.

    “Nevertheless, it displays a general backbone consisting of predominantly α-(1→2)-linked sulfated l-fucose units and, in smaller amounts, α-(1→3)and α-(1→4)-1inked sulfated fucose units (Percival, 1979;Davis et al., 2003;Li et al., 2008;Ale and Meyer, 2013).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Percival, 1979 source

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    • cites Davis et al., 2003 source

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    • cites Li et al., 2008

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    Premisecitation

    Macroalgae accumulate considerable amounts of carbohydrates and thus can be used to produce bioethanol only, not biodiesel.

    “First, in contrast to microalgal feedstocks, which are used for simultaneous production of bioethanol and biodiesel, macroalgae accumulate considerable amounts of carbohydrates, and thus can be used to produce bioethanol only”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Singh et al. (2011); Suutari et al. (2015)

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • May combine two claims.

    Premisecitation

    Cyanobacteria do not accumulate significant amounts of lipids and therefore are not suitable for biodiesel production.

    “For example, in contrast to microalgae, which store high amounts of lipids and carbohydrates, cyanobacteria do not accumulate significant amounts of lipids, and therefore they are not suitable for biodiesel production (Quintana et al., 2011).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Quintana et al., 2011 source

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  • May combine two claims.

    Premisenone given

    Many cyanobacteria, e.g., Spirulina and Synechococcus, accumulate high amounts of glycogen, which can be easily extracted and fermented to ethanol.

    “Among these advantages is the fact that many cyanobacteria, e.g., Spirulina and Synechococcus, accumulate high amounts of glycogen, which can be easily extracted and fermented to ethanol”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Laminarin is synthesized by brown algae and forms either a G-chain with glucose at the reducing end or an M-chain with mannitol at the reducing end.

    “Laminarin is synthesized by brown algae, and it forms either a G-chain -with glucose molecule at the reducing end -or an M-chain -with mannitol at the reducing end (Kadam et al., 2015;Motone et al., 2016).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Kadam et al., 2015;Motone et al., 2016

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Most algae lack the amyloplast and store starch grains in the chloroplast.

    “In contrast to plants, which store starch granules in the amyloplast, most algae lack the amyloplast, and therefore store starch grains in the chloroplast (Busi et al., 2014).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Busi et al., 2014 source

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  • Classified as probably not a substantial claim.

    Interpretationreasoning

    Optimization of the hydrolysis process of structural carbohydrates carries the promise of maximizing ethanol yield.

    “Therefore, optimization of the hydrolysis process of structural carbohydrates carries the promise of maximizing ethanol yield.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Alginate is a linear polysaccharide composed of α-l-guluronate and β-d-mannuronate subunits linked via 1,4-glycosidic bonds and arranged in polyM, polyG, and polyMG blocks.

    “Alginate is a linear polysaccharide composed of α-l-guluronate (G) and β-d-mannuronate (M) subunits.The G and M subunits are linked via 1,4-glycosidic bonds and are arranged in the form of polyM, polyG, and polyMG blocks (Table 2) (Renn, 1997;Draget et al., 2005;Hashimoto et al., 2009).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Renn, 1997 source

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    • cites Draget et al., 2005 source

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    • cites Hashimoto et al., 2009 source

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  • May combine two claims.

    Premisecitation

    Macroalgae accumulate lower amounts of glucan food reserves than microalgae while producing high amounts of non-glucose-based sugars such as mannitol and cell wall polysaccharides.

    “Fourth, macroalgae accumulate lower amounts of glucan food reserves (i.e., glucose-based polysaccharides) in comparison to microalgae, while producing high amounts of non-glucose-based sugars, such as mannitol and cell wall polysaccharides.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Yanagisawa et al., 2013 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Accumulation of high amounts of laminarin in seaweeds can comprise up to 32-35% of dry weight.

    “Accumulation of high amounts of laminarin in algae has been reported in several seaweeds, comprising up to 32-35% of dry weight [refer to Table 1 in Kadam et al. (2015)].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Kadam et al. (2015) source

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  • May combine two claims.

    Premisenone given

    Cellulose is the major algal cell wall polysaccharide and is present in most algal groups.

    “Cellulose is the major algal cell wall polysaccharide, and it is present in most algal groups.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Brown algae accumulate large amounts of mannitol, which functions as an antioxidant and regulator of cell osmolarity.

    “Additionally, brown algae accumulate large amounts of mannitol, which functions as an antioxidant and regulator of cell osmolarity (Davis et al., 2003;Iwamoto and Shiraiwa, 2005).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Davis et al., 2003;Iwamoto and Shiraiwa, 2005

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Agarobiose consists of a d-Gal residue followed by l-AnGal linked by a β-(1→4) glycosidic bond.

    “Agarobiose consists of a d-Gal residue followed by l-AnGal that is linked by a β-(1→4) glycosidic bond.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Renn, 1997 source

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    • cites Fu and Kim, 2010

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    • cites Delattre et al., 2011 source

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  • Probably not a substantial claim: may not pass S4 (based). May combine two claims.

    Premisereasoning

    Food reserves are easily fermented into ethanol and are the primary source for industrial third-generation bioethanol.

    “Food reserves are easily fermented into ethanol and thus are the primary source for industrial third-generation bioethanol.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    93% of the worldwide cultivated macroalgal biomass is produced from four genera: Laminaria 65.8%, Undaria 9.8%, Porphyra 12.6%, and Gracilaria 4.8%.

    “Additionally, 93% of the worldwide cultivated macroalgal biomass is produced from only four genera that belong to the brown algae (Laminaria 65.8% and Undaria 9.8%) and red algae (Porphyra 12.6% and Gracilaria 4.8%) (Zemke-White and Ohno, 1999).”
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    • cites Zemke-White and Ohno, 1999

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  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Premisenone given

    With the exception of diatoms, cellulose is found in the majority of algal cell walls.

    “With exception to diatoms, cellulose is found in the majority of algal cell walls.”
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  • Probably not a substantial claim: may not pass S4 (based).

    Premisenone given

    Hydrolysis of structural carbohydrates is challenging due to their rigidity.

    “In contrast, the hydrolysis of structural carbohydrates is challenging due to their rigidity.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Starch is a homopolysaccharide of glucose units linked by α-(1→4) glycosidic bonds to form linear amylose and by α-(1→6) bonds to form amylopectin.

    “Starch is a homopolysaccharide of glucose units that are linked by α-(1→4) glycosidic bonds to form a linear amylose; and via α-(1→6) bonds to form amylopectin (Table 2) (Fengel and Gert, 1989;Busi et al., 2014).”
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    • cites Fengel and Gert, 1989;Busi et al., 2014

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    Premisecitation

    Fucoidan is a cell wall polysaccharide found in members of family Laminariaceae of brown algae.

    “Fucoidan is a cell wall polysaccharide that is found in the members of family Laminariaceae of brown algae.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Percival, 1979 source

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    • cites Davis et al., 2003 source

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    • cites Li et al., 2008

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Red algae contain agarose and carrageenan, and brown algae are rich in alginate.

    “Such polysaccharides can be specific to an algal group, such as the red algae, which contain agarose and carrageenan; and the brown algae, which are rich in alginate (Vreeland and Kloareg, 2000;Murphy et al., 2013).”
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    • cites Vreeland and Kloareg, 2000;Murphy et al., 2013

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Red algae, Dinophyta, and Glaucophyta store their food reserves in the cytosol.

    “Exceptions to this are the red algae, Dinophyta (Dinoflagellates), and Glaucophyta, which store their food reserves in the cytosol (Radakovits et al., 2010).”
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    • cites Radakovits et al., 2010 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Ulvan is comprised of sulfated rhamnose, glucuronic acid, iduronic acid, xylose, and sulfated xylose.

    “It is comprised of sulfated rhamnose, glucuronic acid, iduronic acid, xylose, and sulfated xylose.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Jiao et al., 2011 source

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    • cites Yanagisawa et al., 2013 source

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    • cites Collén et al., 2014 source

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    Premisecitation

    Carrageenan is a sulfated water-soluble linear galactan of carrabiose or neocarrabiose subunits.

    “Carrageenan is a sulfated water-soluble linear galactan of carrabiose (or neocarrabiose) subunits (Table 2).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites De Ruiter and Rudolph, 1997

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    • cites Renn, 1997 source

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    • cites Delattre et al., 2011 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Agarose is a non-sulfated, non-water-soluble linear galactan composed of repeating disaccharide units of d-galactose and 3,6-anhydro-l-galactose.

    “Agarose is a non-sulfated, non-water-soluble linear galactan that is composed of repeating disaccharide units of d-galactose (d-Gal) and 3,6-anhydro-l-galactose (l-AnGal).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Renn, 1997 source

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    • cites Fu and Kim, 2010

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    • cites Delattre et al., 2011 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Ulvan is a water-soluble cell wall polysaccharide found in green seaweeds such as Ulva and Enteromorpha sp.

    “Ulvan is a water-soluble cell wall polysaccharide, which is found in green seaweeds, such as Ulva and Enteromorpha sp.(Jiao et al., 2011).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Jiao et al., 2011 source

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    Premisecitation

    Degradation of paramylon to glucose is simpler than laminarin and requires the same enzymatic arsenal, with the exception of the debranching endo-β-(1→6) glucanases.

    “Therefore, degradation of paramylon to glucose is simpler than laminarin and requires the same enzymatic arsenal, with the exception of the debranching endo-β-(1→6) glucanases (Takeda et al., 2015).”
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    • cites Takeda et al., 2015 source

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  • May combine two claims.

    Premisenone given

    Simple sugars are readily fermented to ethanol using microbial wild-type strains, whereas fermentation of uronic acid monomers requires genetically engineered microbes that can hydrolyze alginate to KDG and ferment it to ethanol.

    “Simple sugars are readily fermented to ethanol using microbial wild-type strains.In contrast, fermentation of uronic acid monomers requires genetically engineered microbes that can hydrolyze alginate to KDG and ferment it to ethanol.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisereasoning

    Glycogen is similar in structure to amylopectin, and therefore hydrolysis of glycogen requires the same amylolytic enzymes used to break down starch.

    “Glycogen is similar in structure to amylopectin, and therefore the hydrolysis of glycogen requires the same amylolytic enzymes, which are used to breakdown starch.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Aikawa et al., 2013 source

      Not checked in the free run.

    • cites Möllers et al., 2014 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisenone given

    While glucose enters glycolysis directly, galactose must be converted to glucose 6-phosphate via the Leloir pathway before entering glycolysis.

    “While glucose enters glycolysis directly, galactose must be converted to glucose 6-phosphate (glucose-6-P) via the Leloir pathway before entering glycolysis.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Premisenone given

    The hydrolysis of major algal polysaccharides releases several simple sugars, such as glucose, mannose, fructose, galactose, and uronic acids.

    “The hydrolysis of major algal polysaccharides releases several simple sugars, such as glucose, mannose, fructose, galactose, and uronic acids.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Exo-acting β-amylases hydrolyze amylose from the non-reducing ends to produce predominantly maltose, which is cleaved into two glucose residues by glucoamylases.

    “The exo-acting β-amylases (EC 3.2.1.2) hydrolyze amylose from the non-reducing ends to produce predominantly maltose, which is cleaved into two glucose residues by glucoamylases (EC 3.2.1.3)(Figure 2A) [reviewed by Van Zyl et al. (2012)].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Van Zyl et al., 2012 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    At the industrial scale, enzymatic hydrolysis of starch is carried out at elevated temperatures and divided into three steps: starch gelatinization, liquefaction, and saccharification.

    “At the industrial scale, the enzymatic hydrolysis of starch is carried out at elevated temperatures, and it is divided into three steps: starch gelatinization, liquefaction, and saccharification.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Kearsley and Dziedzic, 1995

      Not checked in the free run.

    • cites Kulp and Ponte, 2000

      Not checked in the free run.

    • cites Ratnayake and Jackson, 2009

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationreasoning

    Engineered strains that can ferment several monosaccharides to ethanol will simplify the conversion processes.

    “Therefore, engineered strains, which can ferment several monosaccharides to ethanol, will simplify the conversion processes.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Hydrolysis of algal starch is similar to plant starch degradation steps and requires the same amylolytic enzymes.

    “Hydrolysis of algal starch is similar to plant starch degradation steps and requires the same amylolytic enzymes [for reviews on microbial amylases, refer to Nielsen and Borchert (2000), De Souza and de Oliveira Magalhães (2010), Naidu (2013), Polizeli et al. (2013), and Saranraj and Stella (2013)].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Nielsen and Borchert, 2000

      Not checked in the free run.

    • cites De Souza and de Oliveira Magalhães, 2010

      Not checked in the free run.

    • cites Naidu, 2013

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The major microbial glycolysis pathways are the Embden-Meyerhof-Parnas and the Entner-Doudoroff pathway, depending on the microorganism.

    “The major microbial glycolysis pathways are the Embden-Meyerhof-Parnas (EMP) and the Entner-Doudoroff (ED) pathway, depending on the microorganism [reviewed by Wolfe (2015)].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Wolfe, 2015 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    A plasmid-based E. coli strain capable of simultaneous degradation and fermentation of alginate to ethanol was engineered using alginate metabolic pathway genes from Vibrio splendidus; it fermented 80% of the maximum theoretical yield and produced 0.281 weight ethanol/weight dry macroalgae.

    “Similarly, a plasmid-based E. coli strain, which is capable of simultaneous degradation and fermentation of alginate to ethanol, was engineered using alginate metabolic pathway genes from Vibrio splendidus.This strain, which can metabolize alginate, mannitol, and laminarin, fermented 80% of the maximum theoretical yield and produces 0.281 weight ethanol/weight dry macroalgae (Wargacki et al., 2012”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Wargacki et al., 2012 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The enzymatic breakdown of agarose is carried out by α-agarases and β-agarases, which hydrolyze agarose α-1,3 and β-1,4 linkages and produce agarobiose and neoagarobiose as final hydrolysis products, respectively.

    “The enzymatic breakdown of agarose is carried out by α-agarases (EC 3.2.1.158)and β-agarases (EC 3.2.1.81),which hydrolyze agarose α-1,3 and β-1,4 linkages and produce agarobiose and neoagarobiose as final hydrolysis products, respectively (Table 1).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Fu and Kim, 2010

      Not checked in the free run.

    • cites Chi et al., 2012 source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Interpretationnone given

    One of the major challenges within the context of the enzymatic hydrolysis of algal polysaccharides is to identify hydrolytic enzymes that can break down algal-specific sugars, such as agarose, carrageenan, ulvans, and fucoidan.

    “However, one of the major challenges -within the context of the enzymatic hydrolysis of algal polysaccharides -is to identify hydrolytic enzymes that can breakdown algal-specific sugars, such as agarose, carrageenan, ulvans, and fucoidan.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationnone given

    The hydrolysis process of algal polysaccharides requires more enzymatic mixtures than plants.

    “However the hydrolysis process of algal polysaccharides requires more enzymatic mixtures than plants.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    DEHEP is non-enzymatically rearranged into DEHU, which is reduced to KDG by DEHU reductase.

    “Subsequently, DEHEP is non-enzymatically rearranged into 4-deoxy-l-erythro-5-hexoseulose uronic acid (DEHU), which is reduced to 2-keto-3-deoxy-gluconate (KDG) by DEHU reductase (EC is not available) (Figure 2F) (Wargacki et al., 2012).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Wargacki et al., 2012 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

    Premisenone given

    The classical budding yeast Saccharomyces cerevisiae is the most commonly used microbe for fermenting sugars to bioethanol, and Zymomonas mobilis is used to a lesser extent.

    “The classical budding yeast Saccharomyces cerevisiae is the most commonly used microbe for fermenting sugars to bioethanol.Additionally, the Gram-negative rod-shaped bacterium Zymomonas mobilis is used for fermentation, but to a lesser extent than the budding yeast.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Mannitol is readily dissolved from algal biomass, and therefore conversion of mannitol to ethanol requires no pretreatment steps, which simplifies the bioethanol production process.

    “Mannitol is readily dissolved from algal biomass, and therefore conversion of mannitol to ethanol requires no pretreatment steps, which simplify bioethanol production process (Wang et al., 2013).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Wang et al., 2013 source

      Not checked in the free run.

60 of 60

  • The paper relies on this without support.

    Commercial production of second-generation biofuels is limited to countries with large agricultural and forestry lands.

    “However, commercial production of second-generation biofuels is only limited to countries with large agricultural and forestry lands.”

  • The paper relies on this without support.

    Commercial third-generation biofuels are derived from microalgal biomass.

    “Although commercial third-generation biofuels are derived from microalgal biomass, seaweeds (specifically red and brown macroalgae) serve as an unexploited potential source for bioethanol production due to two facts.”

  • The paper relies on this without support.

    The process of bioethanol production from algal polysaccharides consists of three major steps: biomass pretreatment, enzymatic hydrolysis of algal polysaccharides, and fermentation of sugar monomers to ethanol.

    “The process of bioethanol production from algal polysaccharides consists of three major steps: biomass pretreatment, enzymatic hydrolysis of algal polysaccharides, and fermentation of sugar monomers to ethanol.”

  • The paper relies on this without support.

    The pretreatment step disrupts algal cells and releases intracellular sugars.

    “The pretreatment step disrupts algal cell and releases intracellular sugars.”

  • The paper relies on this without support.

    The pretreatment step reduces algal cell wall crystallinity, making its polysaccharides accessible for enzymatic hydrolysis.

    “Additionally, the pretreatment step reduces algal cell wall crystallinity making its polysaccharides accessible for enzymatic hydrolysis.”

  • The paper relies on this without support.

    Algal biomass is pretreated by physical, chemical, or biological methods.

    “Algal biomass is pretreated by physical, chemical, or biological methods.”

  • The paper relies on this without support.

    Algal biomass is degraded by lytic enzymes into simple sugars and uronic acid monomers.

    “Subsequently, algal biomass is degraded by lytic enzymes into simple sugars and uronic acid monomers.”

  • The paper relies on this without support.

    Simple sugars released during the conversion steps are required for the organism's growth, while ethanol is produced as a byproduct of the fermentation process.

    “Simple sugars, which are released during the conversion steps, are required for the organism's growth, while ethanol is produced as a byproduct of the fermentation process.”

  • The paper relies on this without support.

    Commercial production of ethanol from alginate is challenged by the lack of robust microorganisms that can simultaneously digest, metabolize, and ferment alginate to ethanol at the industrial level.

    “However, the commercial production of ethanol from alginate is challenged by the lack of robust microorganisms that can simultaneously digest, metabolize, and ferment alginate to ethanol at the industrial level.”

  • The paper relies on this without support.

    Algae accumulate high amounts of carbohydrates, which can be used to produce bioethanol.

    “Algae accumulate high amount of carbohydrates, which can be used to produce bioethanol.”
10 of 10

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Paramylon is described both as having and lacking β-(1→6) bonds

    Minor

    The abstract includes paramylon among polysaccharides linked by both β-(1→3) and β-(1→6) bonds, but the body states that paramylon does not form β-(1→6) branches.

1 of 1

The citation lists haven’t been fetched yet

References 131 · Cited by 102

Research works printed but not linked: 5

  1. Bruton, 2009, A Review of the Potential of Marine Algae as a Source of Biofuel in Ireland
  2. Carlsson, 2007, Micro- and Macro-Algae: Utility for Industrial Applications: Outputs from the EPOBIO Project
  3. Dornish, 2006, “Alginate,”, 261
  4. Naidu, 2013, Bacterial amylase a review, Int. J. Pharm. Biol. Arch., 4, 274
  5. Polizeli, 2013, Fungal Enzymes

Authors
Al Abdallah, Q., Nixon, B. T., & Fortwendel, J. R.
Affiliations
  • Pennsylvania State University (US)
  • University of Tennessee Health Science Center (US)
ORCID
Venue
Frontiers in Energy Research
Publisher
Frontiers Media SA
Published
2016-11-04
Volume
4
ISSN
2296-598X (ISSN-L)
DOI
10.3389/fenrg.2016.00036
OpenAlex
W2547449178
Semantic Scholar
17ae72c825fef251c313de9b2205dbdee247d825
Cited by
102
References
131
Citations by year
2026: 3 · 2025: 6 · 2024: 13 · 2023: 8 · 2022: 17 · 2021: 18 · 2020: 13 · 2019: 10 · 2018: 9 · 2017: 4 · 2016: 1
FWCI
3.86
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Frontiers in Energy Research (publishedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
U.S. Department of Energy (DE-SC0006838)
Topics
  • Physical Sciences › Engineering › Biomedical Engineering › Biofuel production and bioconversion
  • Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Algal biology and biofuel production
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Enzyme Production and Characterization
Keywords
bioethanol, algal carbohydrates, cyanobacterial polysaccharides, enzymatic hydrolysis, alginate, laminarin, floridean starch, glycogen, galactose fermentation, Saccharomyces cerevisiae, Zymomonas mobilis, metabolic pathways, genetically modified microorganisms, algal biomass

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