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Cited by 133Algal biology and biofuel productionMicrobial Metabolic Engineering and BioproductionAquatic Ecosystems and Phytoplankton Dynamics

Toward the Enhancement of Microalgal Metabolite Production through Microalgae–Bacteria Consortia

Open access
González-González, Lina Maria, de-Bashan, Luz E.·2021·Biology
DOI 10.3390/biology10040282PMC PMC8065533
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Abstract

Engineered mutualistic consortia of microalgae and bacteria may be a means of assembling a novel combination of metabolic capabilities with potential biotechnological advantages. Microalgae are promising organisms for the sustainable production of metabolites of commercial interest, such as lipids, carbohydrates, pigments, and proteins. Several studies reveal that microalgae growth and cellular storage of these metabolites can be enhanced significantly by co-cultivation with growth-promoting bacteria. This review summarizes the state of the art of microalgae–bacteria consortia for the production of microalgal metabolites. We discuss the current knowledge on microalgae–bacteria mutualism and the mechanisms of bacteria to enhance microalgae metabolism. Furthermore, the potential routes for a microalgae–bacteria biorefinery are outlined in an attempt to overcome the economic failures and negative energy balances of the existing production processes.

AI snapshot

Written from the paper’s full text.

TL;DR

This review summarizes how mutualistic microalgae–bacteria consortia can enhance microalgal biomass and metabolite production, including lipids, carbohydrates, pigments, and proteins. It also outlines how growth-promoting bacteria could improve microalgae biorefineries through harvesting, CO2 fixation, wastewater treatment, and residual biomass valorization.

Key findings

  • Co-cultivation with growth-promoting bacteria can increase microalgal growth and biomass: wastewater-isolated bacteria enhanced *C. reinhardtii*, *C. vulgaris*, and *Euglena gracilis* growth up to 2.8-fold; *Pelagibaca bermudensis* enhanced *Tetraselmis striata* biomass productivity two-fold; four bacterial strains increased *C. vulgaris* population by more than 100%.
  • Lipid production is commonly enhanced: *C. reinhardtii* co-cultured with *Azotobacter chroococcum* under nitrogen starvation showed 2.4-fold higher lipid content, 5.9-fold higher lipid production, and up to 19.4-fold higher lipid productivity than axenic cultures; *C. vulgaris* with *A. brasilense* reached up to five-fold higher lipids under autotrophic conditions.
  • Carbohydrate and pigment yields also increase: *C. vulgaris* co-cultivated with *A. brasilense* showed up to 72% and 90% increments in total carbohydrates under autotrophic and heterotrophic conditions, while co-immobilization with *A. brasilense* increased chlorophyll a by up to 35%, chlorophyll b by 176%, β-carotene by 186%, lutein by 152%, and violaxanthin by 129%.
  • Bacteria may improve biorefinery steps: *Bacillus* sp. aggregation of *Nannochloropsis oceanica* reached up to 95% efficiency in 30 s; *A. brasilense* improved CO2 fixation by 25–50% in *S. obliquus*, 46–87% in *C. vulgaris*, and 41–53% in *C. reinhardtii* under high CO2; leachate treatment removed 100% ammonium and up to 90% nitrate, COD, and phenol.

Methods

  • Narrative review of the state of the art on microalgae–bacteria consortia for microalgal metabolite production, mutualistic mechanisms, and biorefinery routes.
  • Synthesizes published studies on synthetic and natural co-cultures, including co-cultivation, immobilization, bacterial extracts/volatiles, omics, nanoSIMS, and wastewater/biorefinery applications.
  • Main analysis is qualitative synthesis, with tables and figures summarizing reported effects on biomass, lipids, carbohydrates, pigments, proteins, harvesting, CO2 fixation, and nutrient removal; no new experimental data are presented.

Limitations

  • The paper states that genomic, transcriptomic, and metabolomic studies in synthetic mutualistic consortia are currently very limited, and that no studies to the authors’ knowledge evaluate microalgae–bacteria consortia in integrated microalgal biorefineries.
  • The paper notes that less attention has been paid to bacterial enhancement of microalgal pigments, carbohydrates, and proteins than to lipids.
  • Evident from the text: as a narrative review, it lacks a systematic search strategy or quantitative meta-analysis, and it compares findings from diverse species, co-culture setups, and cultivation conditions, which limits direct comparability.

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Integrity signals

Registry

Crossref · 10.3390/biology10040282

Cites

148 of 148 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 89 cited sources checked · 0 supported · 0 flagged

  • Premisecitation

    The mechanisms involved in microalgae-bacteria interaction seem to be species-specific, depending on the microenvironment and conditions of each microalga.

    “However, the mechanisms involved in the interaction do seem to be species-specific, depending on the microenvironment and conditions of each microalga [11].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [11] Ramanan, 2016, Algae-bacteria interactions: Evolution, ecology and emerging applications, Biotechnol. Adv. source

      Not checked in the free run.

  • Interpretationnone given

    Engineered mutualistic consortia of microalgae and bacteria may assemble a novel combination of metabolic capabilities with potential biotechnological advantages.

    “Engineered mutualistic consortia of microalgae and bacteria may be a means of assembling a novel combination of metabolic capabilities with potential biotechnological advantages.”
    Quote in the paperSubstantial claim
  • Premisecitation

    It is possible to construct a synthetic mutualism using two species or strains that do not interact in nature.

    “However, through the use of two species or strains that do not interact in nature, it is possible to construct a synthetic mutualism [25].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [25] Kubo, 2013, Construction of bacteria–eukaryote synthetic mutualism, Biosystems source

      Not checked in the free run.

  • Interpretationcitation

    Microalgae growth and cellular storage of metabolites such as lipids, carbohydrates, pigments, and proteins can be enhanced significantly by co-cultivation with growth-promoting bacteria.

    “Several studies reveal that microalgae growth and cellular storage of these metabolites can be enhanced significantly by co-cultivation with growth-promoting bacteria.”
    • Also stated in: § 3. Enhancement of Biomass and Metabolite Production · plain
      “The cultivation of microalgae with growth-promoting bacteria results not just in the enhancement of biomass production but also in the increment of the intracellular levels of lipids, carbohydrates, pigments, and proteins (Table 2).”
    Quote in the paperSubstantial claim
  • Premisecitation

    The inoculation ratios of microorganisms play an important role in the performance of the synthetic consortium.

    “The inoculation ratios of the microorganisms play an important role in the performance of the synthetic consortium [28,29].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [28] Nguyen, 2020, Co-culture of microalgae-activated sludge for wastewater treatment and biomass production: Exploring their role under different inoculation ratios, Bioresour. Technol. source

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    • cites [29] Su, 2012, Synergistic cooperation between wastewater-born algae and activated sludge for wastewater treatment: Influence of algae and sludge inoculation ratios, Bioresour. Technol. source

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  • May combine two claims. 35
  • Classified as probably not a substantial claim. 8

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    Premisecitation

    Nearly 50% of microalgae are auxotrophs for vitamin B12 (cobalamin) and 22% for vitamin B1 (thiamine).

    “Nearly 50% of microalgae are auxotrophs for vitamin B12 (cobalamin) and 22% for vitamin B1 (thiamine).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [23] Cooper, 2015, Exploring mutualistic interactions between microalgae and bacteria in the omics age, Curr. Opin. Plant Biol. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Microalgae-bacteria consortia have been explored as an alternative route to enhancing microalgae growth and metabolite production because growth-promoting factors are produced by bacteria.

    “Since these growth-promoting factors are produced by bacteria, microalgae–bacteria consortia have been explored as an alternative route to enhancing microalgae growth and metabolite production [9,10].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [9] Yao, 2019, Microalgae–bacteria symbiosis in microalgal growth and biofuel production: A review, J. Appl. Microbiol. source

      Not checked in the free run.

    • cites [10] Fuentes, J.L., Garbayo, I., Cuaresma, M., Montero, Z., Gonzalez-Del-Valle, M., and Vilchez, C. (2016). Impact of microalgae-bacteria interactions on the production of algal biomass and associated compounds. Mar. Drugs, 14. source

      Not checked in the free run.

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    Premisecitation

    Microalgae exude photosynthesized organics as dissolved organic carbon (DOC); heterotrophic bacteria assimilate them, and in return bacteria contribute to algal growth through generation of CO2, micronutrients such as Fe, vitamins, macronutrients specifically fixed N, and phytohormones.

    “Microalgae exude a part of the photosynthesized organics as dissolved organic carbon (DOC); these are assimilated by heterotrophic bacteria, and in return, bacteria contribute to algal growth through the generation of CO2, micronutrients (such as Fe), vitamins, macronutrients, specifically fixed N and phytohormones [15,17].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [15] Croft, 2005, Algae acquire vitamin B12 through a symbiotic relationship with bacteria, Nature source

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    • cites [17] Samo, 2018, Attachment between heterotrophic bacteria and microalgae influences symbiotic microscale interactions, Environ. Microbiol. source

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    Premisecitation

    Attachment defines a differential response in cell-cell exchange: 92-98% of P. tricornutum cells had attached bacteria and fixed 64% more carbon than axenic cells, whereas only 42-63% of N. salina cells had associations and fixed just 10% more carbon.

    “The authors reported that attachment defines a differential response, while 92–98% of cells of P. tricornutum had attached bacteria and fixed 64% more carbon than axenic cells. In contrast, only 42–63% of N. salina cells had associations with bacteria and fixed just 10% more carbon compared to axenic cells.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [17] Samo, 2018, Attachment between heterotrophic bacteria and microalgae influences symbiotic microscale interactions, Environ. Microbiol. source

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    Interpretationcitation

    The co-culture induces some stress in L. rostrata, and it must adjust its metabolism accordingly.

    “Despite the stability of this synthetic mutualism, the responses of L. rostrata show that the co-culture induces some stress in the microalga, and it must adjust its metabolism accordingly [47].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [47] Helliwell, 2018, Quantitative proteomics of a B12 -dependent alga grown in coculture with bacteria reveals metabolic tradeoffs required for mutualism, New Phytol. source

      Not checked in the free run.

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    Premisecitation

    The transfer of carbon and nitrogen compounds between C. sorokiniana and A. brasilense was demonstrated; bacteria significantly enhanced growth of microalgae, while microalgae supported growth of bacteria in a medium where it could not otherwise grow.

    “The transfer of carbon and nitrogen compounds between the two organisms was demonstrated by de-Bashan et al. [27]; the bacteria significantly enhanced the growth of the microalgae, while the microalgae supported the growth of the bacteria in a medium where it could not otherwise grow.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [27] Mayali, 2016, Establishment of stable synthetic mutualism without co-evolution between microalgae and bacteria demonstrated by mutual transfer of metabolites (NanoSIMS isotopic imaging) and persistent physical association (Fluorescent in situ hybridization), Algal Res. source

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    Premisecitation

    Vitamin B12 is produced only by prokaryotes and is the source of the vitamin for the microalga in exchange for photosynthates.

    “As vitamin B12 is produced only by prokaryotes, it is the source of the vitamin for the microalga in exchange for photosynthates [23].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [23] Cooper, 2015, Exploring mutualistic interactions between microalgae and bacteria in the omics age, Curr. Opin. Plant Biol. source

      Not checked in the free run.

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    Premisecitation

    Cultivation of Dunaliella bardawil with Halomonas sp. under iron deficiency increased Fe solubility, enhancing its availability to algae and significantly improving algal growth rate.

    “The cultivation of Dunaliella bardawil with Halomonas sp. isolated from algae cultures highlighted the siderophores’ key role in microalgal growth under iron deficiency. The bacteria increased Fe solubility, in this way enhancing its availability to the algae, which in turn significantly improved the algal growth rate [56].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [56] Hadar, 1995, Oligotrophic bacteria enhance algal growth under iron-deficient conditions, Appl. Environ. Microbiol. source

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    Premisecitation

    In co-culture, the thiamine producer Pseudoalteromonas sp. allows growth of the marine thiamine auxotroph Ostreococcus lucimarinus, and Dinoroseobacter shibae provides vitamins B1 and B12 to its dinoflagellate host.

    “in co-culture, the thiamine producer Pseudoalteromonas sp. allows the growth of the marine thiamine auxotroph microalgae Ostreococcus lucimarinus [48], and the marine bacterium Dinoroseobacter shibae, isolated from the benthic dinoflagellate Prorocentrum lima, provides vitamins B1 and B12 to its dinoflagellate host [49].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [48] Paerl, 2015, Vitamin B1 ecophysiology of marine picoeukaryotic algae: Strain-specific differences and a new role for bacteria in vitamin cycling, Limnol. Oceanogr. source

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    • cites [49] Ballhausen, 2010, The complete genome sequence of the algal symbiont Dinoroseobacter shibae: A hitchhiker’s guide to life in the sea, ISME J. source

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    Premisecitation

    M. loti supplies vitamin B12 to L. rostrata, and in return receives fixed carbon from the microalga.

    “A model interaction for the exchange of vitamin B12 is the one created between the soil rhizobiaceae Mesorhizobium loti and the freshwater green microalga Lobomonas rostrata, where M. loti supplies vitamin B12, and in return, the bacterium receives fixed carbon from the microalga [45,46,47].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [45] Kazamia, 2012, Mutualistic interactions between vitamin B12-dependent algae and heterotrophic bacteria exhibit regulation, Environ. Microbiol. source

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    • cites [46] Grant, 2014, Direct exchange of vitamin B 12 is demonstrated by modelling the growth dynamics of algal–bacterial cocultures, ISME J. source

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    • cites [47] Helliwell, 2018, Quantitative proteomics of a B12 -dependent alga grown in coculture with bacteria reveals metabolic tradeoffs required for mutualism, New Phytol. source

      Not checked in the free run.

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    Premisecitation

    Co-cultivation of C. reinhardtii with Azotobacter chroococcum under nitrogen starvation increased lipid content 2.4 times, lipid production 5.9 times, and lipid productivity up to 19.4 times compared with axenic microalga.

    “The authors reported an increase of 2.4 times in lipid content and 5.9 times in lipid production with the co-culture and up to 19.4 times the lipid productivity compared with the axenic microalga.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [83] Xu, 2018, Enhanced lipid production in Chlamydomonas reinhardtii by co-culturing with Azotobacter chroococcum, Front Plant Sci. source

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  • May combine two claims.

    Premisecitation

    M. loti regulates production of cobalamin according to the requirements of the microalga rather than simply releasing nutrients to the medium, creating a true mutualistic interaction with L. rostrata.

    “Mathematical models that analyze the nutrient exchange between the microorganisms showed that M. loti regulates the production of cobalamin according to the requirements of the microalga rather than simply releasing nutrients to the medium, in this way creating a true mutualistic interaction with L. rostrata [46].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [46] Grant, 2014, Direct exchange of vitamin B 12 is demonstrated by modelling the growth dynamics of algal–bacterial cocultures, ISME J. source

      Not checked in the free run.

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    Premisecitation

    A. brasilense produces riboflavin and lumichrome, and both compounds affect growth and metabolism of Chlorella sorokiniana.

    “Lopez et al. [41] reported that A. brasilense produces riboflavin and lumichrome (a compound produced by the light degradation of riboflavin, which is also suggested as a plant-growth promoter), and both compounds affect the growth and metabolism of Chlorella sorokiniana.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [41] Lopez, 2019, Riboflavin and lumichrome exuded by the bacterium Azospirillum brasilense promote growth and changes in metabolites in Chlorella sorokiniana under autotrophic conditions, Algal Res. source

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    Premisecitation

    C. vulgaris cultivated with Stenotrophomonas maltophilia produced more than 80% C16 and C18 in fatty acids, an increase of up to 5% compared to axenic cultures.

    “Xue et al. [83] reported more than 80% content of C16 and C18 in the fatty acids produced by the microalga C. vulgaris when cultivated with Stenotrophomonas maltophilia as well as an increase of up to 5% when compared to axenic cultures.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [83] Xu, 2018, Enhanced lipid production in Chlamydomonas reinhardtii by co-culturing with Azotobacter chroococcum, Front Plant Sci. source

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    Premisecitation

    In co-cultures of three Chlorella strains with A. brasilense immobilized in alginate beads, concentration and variety of fatty acids increased, reaching up to eight different fatty acids compared to four to five in microalgae-only immobilized cells.

    “In all the co-cultures, the concentration and variety of fatty acids increased, reaching up to eight different fatty acids in microalgae co-immobilized with the MGPB in comparison to four to five in microalgae-only immobilized cells.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [75] Bashan, 2002, Increased pigment and lipid content, lipid variety, and cell and population size of the microalgae Chlorella spp. when co-immobilized in alginate beads with the microalgae-growth-promoting bacterium Azospirillum brasilense, Can. J. Microbiol. source

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    Premisecitation

    At 1% substrate concentration, the total starch productivity as well as lipid productivity increased in all the co-cultures compared to axenic conditions.

    “At 1% substrate concentration, the total starch productivity as well as lipid productivity increased in all the co-cultures compared to axenic conditions.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [72] Higgins, B.T., and Vandergheynst, J.S. (2014). Effects of Escherichia coli on mixotrophic growth of Chlorella minutissima and production of biofuel precursors. PLoS ONE, 9. source

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    Premisecitation

    The co-immobilization of the microorganisms resulted in increments of up to 35% in chlorophyll a, 176% in chlorophyll b, 186% in ß-carotene, 152% in lutein, and 129% in violaxanthin.

    “The co-immobilization of the microorganisms resulted in increments of up to 35% in chlorophyll a, 176% in chlorophyll b, 186% in ß-carotene, 152% in lutein, and 129% in violaxanthin [87].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [87] Gonzalez, 2000, Increased growth of the microalga Chlorella vulgaris when coimmobilized and cocultured in alginate beads with the plant-growth-promoting bacterium Azospirillum brasilense, Appl. Environ. Microbiol. source

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    Premisecitation

    The use of wastewater as the culture medium for microalgae may reduce the use of commercial fertilizers and at the same time minimize freshwater consumption.

    “The use of wastewater as the culture medium for microalgae may reduce the use of commercial fertilizers and at the same time minimize freshwater consumption [95,96,97].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [95] Safafar, 2015, Carotenoids, phenolic compounds and tocopherols contribute to the antioxidative properties of some microalgae species grown on industrial wastewater, Mar. Drugs source

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    • cites [96] Zhou, 2015, Biomass and pigments production in photosynthetic bacteria wastewater treatment: Effects of photoperiod, Bioresour. Technol. source

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    • cites [97] Zhou, 2014, Biomass and carotenoid production in photosynthetic bacteria wastewater treatment: Effects of light intensity, Bioresour. Technol. source

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    Premisecitation

    C. sorokiniana had an increase in carbohydrate production of around 55% under autotrophic conditions and 21% under heterotrophic conditions.

    “while C. sorokiniana had an increase in carbohydrate production of around 55% under autotrophic conditions and 21% under heterotrophic conditions.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [70] Choix, 2012, Enhanced accumulation of starch and total carbohydrates in alginate-immobilized Chlorella spp. induced by Azospirillum brasilense: I. Autotrophic conditions, Enzym. Microb. Technol. source

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    • cites [79] Choix, 2012, Enhanced accumulation of starch and total carbohydrates in alginate-immobilized Chlorella spp. induced by Azospirillum brasilense: II. Heterotrophic conditions, Enzym. Microb. Technol. source

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    Premisecitation

    The authors reported 100% removal of ammonium and up to 90% removal efficiencies for nitrate, chemical oxygen demand, and phenol.

    “The authors reported 100% removal of ammonium and up to 90% removal efficiencies for nitrate, chemical oxygen demand, and phenol.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [102] Tighiri, 2019, Biotreatment of landfill leachate by microalgae-bacteria consortium in sequencing batch mode and product utilization, Bioresour. Technol. source

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    Premisecitation

    Powell and Hill explored this way of aggregating algae by cultivating Nannochloropsis oceanica with the bacterium Bacillus sp., reaching up to 95% efficiency, with aggregates formed in 30 s.

    “Powell and Hill [124] explored this way of aggregating algae by cultivating Nannochloropsis oceanica with the bacterium Bacillus sp., reaching up to 95% efficiency, with aggregates formed in 30 s.”
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    • cites [124] Powell, 2013, Rapid aggregation of biofuel-producing algae by the bacterium Bacillus sp. strain RP1137, Appl. Environ. Microbiol. source

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

    Premisecitation

    The use of microalgae-bacteria consortia in wastewater treatment has been widely studied, revealing that the microbial community plays an important role on the performance of the system.

    “Therefore, the use of microalgae–bacteria consortia in wastewater treatment has been widely studied, revealing that the microbial community plays an important role on the performance of the system [98,99,100].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [98] Paddock, 2020, The effect of the microalgae-bacteria microbiome on wastewater treatment and biomass production, Appl. Microbiol. Biotechnol. source

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    • cites [99] Solimeno, 2017, Microalgae-bacteria models evolution: From microalgae steady-state to integrated microalgae-bacteria wastewater treatment models–a comparative review, Sci. Total Environ. source

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    • cites [100] Jia, 2016, Removal of nitrogen from wastewater using microalgae and microalgae–bacteria consortia, Cogent Environ. Sci. source

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    Premisecitation

    The harvested biomass contained around 23% lipid content, including fatty acid methyl esters optimal for biodiesel production.

    “The harvested biomass contained around 23% lipid content, including fatty acid methyl esters optimal for biodiesel production.”
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    • cites [118] Bohutskyi, 2019, Production of lipid-containing algal-bacterial polyculture in wastewater and biomethanation of lipid extracted residues: Enhancing methane yield through hydrothermal pretreatment and relieving solvent toxicity through co-digestion, Sci. Total Environ. source

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    Premisecitation

    The results showed that growth and lipid production was the same or higher when compared to the standard medium.

    “The results showed that growth and lipid production was the same or higher when compared to the standard medium, which implies significant savings in the production process.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [103] Tremblay, 2018, Cultivation of an algae-bacteria consortium in wastewater from an industrial park: Effect of environmental stress and nutrient deficiency on lipid production, Bioresour. Technol. source

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    Premisecitation

    The relative toxicity was reduced from 57.32 to 1.12%, while the fatty acid content (C16-18) reached up to 88% of the biomass.

    “Furthermore, the relative toxicity was reduced from 57.32 to 1.12%, while the fatty acid content (C16–18) reached up to 88% of the biomass.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [102] Tighiri, 2019, Biotreatment of landfill leachate by microalgae-bacteria consortium in sequencing batch mode and product utilization, Bioresour. Technol. source

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    Premisecitation

    Although methane production of the lipid-extracted biomass was low (296 ± 2 mL/gVS), the biomethane potential was maximized by hydrothermal liquefaction pretreatment and co-digestion with sewage sludge.

    “Although methane production of the lipid-extracted biomass was low (296 ± 2 mL/gVS), the biomethane potential was maximized by hydrothermal liquefaction pretreatment (to increase biomass biodegradability) and co-digestion with sewage sludge (to reduce toxicity due to solvent residues).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [118] Bohutskyi, 2019, Production of lipid-containing algal-bacterial polyculture in wastewater and biomethanation of lipid extracted residues: Enhancing methane yield through hydrothermal pretreatment and relieving solvent toxicity through co-digestion, Sci. Total Environ. source

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    Premisecitation

    The maximum hydrogen yield was found with the cultivation of the hydrogenase-deficient E. coli.

    “The maximum hydrogen yield was found with the cultivation of the hydrogenase-deficient E. coli.”
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    • cites [113] Lakatos, 2014, Bacterial symbionts enhance photo-fermentative hydrogen evolution of Chlamydomonas algae, Green Chem. source

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    Premisecitation

    The MGPB A. brasilense and Bacillus pumilus remotely enhanced microalgal growth as well as lipids, carbohydrates, and chlorophyll a production.

    “The MGPB A. brasilense and Bacillus pumilus remotely enhanced microalgal growth as well as lipids, carbohydrates, and chlorophyll a production [42].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [42] Amavizca, 2017, Enhanced performance of the microalga Chlorella sorokiniana remotely induced by the plant growth-promoting bacteria Azospirillum brasilense and Bacillus pumilus, Sci. Rep. source

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    Premisecitation

    The cultivation of the microalgae Characium sp. in the cell-free filtrate of Pseudomonas composti resulted in an increase of 57% in the microalgal biomass, while lipid productivity increased by 18%.

    “For instance, the cultivation of the microalgae Characium sp. in the cell-free filtrate of Pseudomonas composti resulted in an increase of 57% in the microalgal biomass, while lipid productivity increased by 18% [40].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [40] Berthold, 2019, Enhancing algal biomass and lipid production through bacterial co-culture, Biomass Bioenergy source

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    Premisecitation

    The application of the dry beads increased organic matter, organic carbon, and microbial carbon in the soil.

    “The application of the dry beads increased organic matter, organic carbon, and microbial carbon in the soil.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [135] Trejo, 2012, Recycling waste debris of immobilized microalgae and plant growth-promoting bacteria from wastewater treatment as a resource to improve fertility of eroded desert soil, Environ. Exp. Bot. source

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    • cites [136] Lopez, 2013, Amendment of degraded desert soil with wastewater debris containing immobilized Chlorella sorokiniana and Azospirillum brasilense significantly modifies soil bacterial community structure, diversity, and richness, Biol. Fertil. Soils source

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    Premisecitation

    The non-negligible cost of production related to microalgae CO2 consumption can be significantly reduced, not just through the CO2 generated from the bacterial partner but also by using CO2 emissions from industrial plants in the cultivation systems or through biogas upgrading.

    “The non-negligible cost of production related to microalgae CO2 consumption can be significantly reduced, not just through the CO2 generated from the bacterial partner but also by using CO2 emissions from industrial plants in the cultivation systems [138,139] or through biogas upgrading [140].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [138] 2016, Optimal design of distributed algae-based biorefineries using CO2 emissions from multiple industrial plants, Ind. Eng. Chem. Res. source

      Not checked in the free run.

    • cites [139] Franco, 2010, Microalgae-based systems for carbon dioxide sequestration and industrial biorefineries, Biomass. Croat. Sciyo

      Not checked in the free run.

    • cites [140] Nagarajan, 2019, Integration of anaerobic digestion and microalgal cultivation for digestate bioremediation and biogas upgrading, Bioresour. Technol. source

      Not checked in the free run.

    • Rests on an assumption: The cost of production related to microalgae CO2 consumption is non-negligible.

  • May combine two claims.

    Premisecitation

    Cho et al. cultivated C. vulgaris with isolated bacteria from the same culture and observed that the artificial microalgae-bacteria consortia had flocculation efficiency, lipid content, and quality superior to that of the axenic microalgae culture.

    “Likewise, Cho et al. [81] cultivated C. vulgaris with isolated bacteria from the same culture and observed that the artificial microalgae–bacteria consortia had flocculation efficiency, lipid content, and quality superior to that of the axenic microalgae culture.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [81] Cho, 2015, Enhancing microalgal biomass productivity by engineering a microalgal-bacterial community, Bioresour. Technol. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Application of the beads significantly changed the rhizosphere bacterial population structure, and species richness and diversity increased with the beads containing the microalgae-bacteria association.

    “Application of the beads significantly changed the rhizosphere bacterial population structure, and species richness and diversity increased with the beads containing the microalgae–bacteria association [135,136].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [135] Trejo, 2012, Recycling waste debris of immobilized microalgae and plant growth-promoting bacteria from wastewater treatment as a resource to improve fertility of eroded desert soil, Environ. Exp. Bot. source

      Not checked in the free run.

    • cites [136] Lopez, 2013, Amendment of degraded desert soil with wastewater debris containing immobilized Chlorella sorokiniana and Azospirillum brasilense significantly modifies soil bacterial community structure, diversity, and richness, Biol. Fertil. Soils source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing), S4 (based). May combine two claims.

    Interpretationnone given

    Although genomic, transcriptomic, and metabolomic studies in synthetic mutualistic consortia are currently very limited, they are of utmost importance in understanding the underlying mechanisms acting in establishing and stabilizing the mutualism.

    “Thus, although genomic, transcriptomic, and metabolomic studies in synthetic mutualistic consortia are currently very limited, they are of utmost importance in understanding the underlying mechanisms acting in establishing and stabilizing the mutualism.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Genomic, transcriptomic, and metabolomic studies in synthetic mutualistic consortia are currently very limited.

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

    Interpretationcitation

    The development of circular economy principle-based systems, such as microalgae-bacteria consortia biorefineries, constitutes an option to reduce CO2 emissions within the framework of meeting the international COP21 Paris CO2 emission reduction commitments and UN Sustainable Development Goals.

    “Lastly, the development of circular economy principle-based systems, such as microalgae–bacteria consortia biorefineries, constitutes an option to reduce CO2 emissions within the framework of meeting the international COP21 Paris CO2 emission reduction commitments and UN Sustainable Development Goals [148].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [148] Mccollum, 2018, Connecting the sustainable development goals by their energy inter-linkages, Environ. Res. Lett. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based).

    Interpretationreasoning

    The development of microalgal biorefineries based on mutualistic interaction between growth-promoting bacteria and microalgae stands as an attractive alternative in overcoming the drawbacks that currently jeopardize the application of these biorefineries on a large scale.

    “The development of microalgal biorefineries based on mutualistic interaction between growth-promoting bacteria and microalgae stands as an attractive alternative in overcoming the drawbacks that currently jeopardize the application of these biorefineries on a large scale.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The cost of production of microalgae-based proteins, lipids, pigments, and carbohydrates is a bottleneck that prevents many industries from shifting to sustainable production.

  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based).

    Interpretationreasoning

    Knowing each of the partners' specific nutritional and environmental requirements can help the manipulation of the intended biotechnological response.

    “Knowing each of the partners’ specific nutritional and environmental requirements can help the manipulation of the intended biotechnological response.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    The results revealed that A. brasilense has the ability to mitigate the stress caused by CO2 levels of up to 35%, improving the CO2 fixation rate by 25-50% in S. obliquus, 46-87% in C. vulgaris, and 41-53% in C. reinhardtii.

    “The results revealed that A. brasilense has the ability to mitigate the stress caused by CO2 levels of up to 35%, improving the CO2 fixation rate by 25–50% in S. obliquus, 46–87% in C. vulgaris, and 41–53% in C. reinhardtii.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [63] Choix, 2018, Azospirillum brasilense increases CO2 fixation on microalgae Scenedesmus obliquus, Chlorella vulgaris, and Chlamydomonas reinhardtii cultured on high CO2 concentrations, Microb. Ecol. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based).

    Interpretationreasoning

    The demonstration of mutual benefits and the association's self-maintenance duration over several consecutive generations is fundamental to the validation of this approach.

    “The demonstration of mutual benefits and the association’s self-maintenance duration over several consecutive generations is fundamental to the validation of this approach.”
    Quote in the paperNot a substantial claim

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

    Interpretationnone given

    A successful microalgae-bacteria consortia must be beneficial to all microorganisms.

    “In summary, a successful microalgae-bacteria consortia must be beneficial to all microorganisms.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Production costs associated with fertilizer consumption can be minimized either by using wastewater as the culture medium, or by recycling the main nutrients, such as nitrogen and phosphorous recovered after anaerobic digestion or hydrothermal liquefaction conversion.

    “Besides, as stated before, production costs associated with fertilizer consumption can be minimized either by using wastewater as the culture medium, or by recycling the main nutrients, such as nitrogen and phosphorous recovered after anaerobic digestion [142,143,144] or hydrothermal liquefaction conversion [145,146].”
    Quote in the paperNot a substantial claim0 of 5 sources checked
    • cites [142] Sforza, 2017, Anaerobic digestion of lipid-extracted microalgae: Enhancing nutrient recovery towards a closed loop recycling, Biochem. Eng. J. source

      Not checked in the free run.

    • cites [143] 2015, Production of microalgae using centrate from anaerobic digestion as the nutrient source, Algal Res. source

      Not checked in the free run.

    • cites [144] Eltanahy, 2019, Assessing the fertilizing potential of microalgal digestates using the marine diatom Chaetoceros muelleri, Algal Res. source

      Not checked in the free run.

    • cites [145] Barreiro, 2015, Cultivation of microalgae with recovered nutrients after hydrothermal liquefaction, Algal Res. source

      Not checked in the free run.

    • cites [146] Biller, 2012, Nutrient recycling of aqueous phase for microalgae cultivation from the hydrothermal liquefaction process, Algal Res. source

      Not checked in the free run.

41 of 41

  • The paper relies on this without support.

    The mechanisms involved in a synthetic mutualistic interaction between microalgae and bacteria are similar to those found in natural associations.

    “The mechanisms involved in a synthetic mutualistic interaction between microalgae and bacteria are similar to those found in natural associations.”

  • The authors state this as an assumption.

    The bacteria grow at the expense of the photosynthates produced by the microalga in the Croft et al. experiment.

    “Because the medium where these two microorganisms were growing did not contain any organic carbon source, it is logical to assume that the bacteria grow at the expense of the photosynthates produced by the microalga.”

  • The paper relies on this without support.

    Nutrient exchange is the most common and important type of mutualistic interaction between microalgae and bacteria.

    “In general, nutrient exchange has been considered the most common and important.”

  • The paper relies on this without support.

    The cost of production of microalgae-based proteins, lipids, pigments, and carbohydrates is a bottleneck that prevents many industries from shifting to sustainable production.

    “The cost of production of microalgae-based proteins, lipids, pigments, and carbohydrates is still a bottleneck that prevents many industries from making this desirable shift.”

  • The paper relies on this without support.

    No studies are evaluating microalgae–bacteria consortia in these kinds of biorefineries.

    “Although, as we described earlier, growth-promoting bacteria can significantly enhance the production of these metabolites; to the authors’ knowledge, no studies are evaluating microalgae–bacteria consortia in these kinds of biorefineries.”

  • The paper relies on this without support.

    Natural bacterial communities in wastewater effluents are a combination of beneficial and competing species.

    “Because the natural bacterial communities in wastewater effluents are a combination of beneficial and competing species, artificial consortia are preferred to boost microalgal biomass production.”

  • The paper relies on this without support.

    The viability of bacteria after metabolite extraction depends on the target metabolite and the extraction process.

    “The viability of bacteria after metabolite extraction depends on the target metabolite and the extraction process.”

  • The paper relies on this without support.

    The cost of production related to microalgae CO2 consumption is non-negligible.

    “The non-negligible cost of production related to microalgae CO2 consumption can be significantly reduced”

  • The paper relies on this without support.

    Genomic, transcriptomic, and metabolomic studies in synthetic mutualistic consortia are currently very limited.

    “Thus, although genomic, transcriptomic, and metabolomic studies in synthetic mutualistic consortia are currently very limited, they are of utmost importance in understanding the underlying mechanisms acting in establishing and stabilizing the mutualism.”
9 of 9

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.

  • Reference [83] is attributed to two different studies

    Minor

    The text first uses [83] for co-cultivation of C. reinhardtii with Azotobacter chroococcum, then attributes to it results for C. vulgaris with Stenotrophomonas maltophilia. The reference list identifies [83] as the former study, so the later attribution is inconsistent.

1 of 1

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Related

Authors
González-González, L. M., & de-Bashan, L. E.
Affiliations
The Bashan Institute of Science, 1730 Post Oak Ct, Auburn, AL 36830, USA
ORCID
González-González, Lina Maria
Venue
Biology
Publisher
MDPI AG
Published
2021-04-01
Volume
10
Issue
4
Pages
282
ISSN
2079-7737 (ISSN-L)
DOI
10.3390/biology10040282
PMC
PMC8065533
OpenAlex
W3143606184
Cited by
133
References
149
Citations by year
2026: 21 · 2025: 34 · 2024: 29 · 2023: 19 · 2022: 22 · 2021: 8
FWCI
0.96
Type
journal article
Language
en
Open access
Licence
Locations
  • Biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Algal biology and biofuel production
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
  • Physical Sciences › Environmental Science › Environmental Chemistry › Aquatic Ecosystems and Phytoplankton Dynamics
Keywords
microalgae-bacteria consortia, co-culture, growth-promoting bacteria, lipid production, carbohydrate production, pigments, microalgal proteins, biorefinery, energy balance

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