Review
Sustainable production of algae-bacteria granular consortia based biological hydrogen: New insights

https://doi.org/10.1016/j.biortech.2022.127036Get rights and content

Highlights

  • Process of microbial granule formation and microbial components of mature granules.

  • Important enzymes useful in the Hydrogen production have ben briefly discussed.

  • Granular Hydrogen productions by different type of granules have been tabulated.

  • Molecular engineering and other options for improving H2 production.

Abstract

Microbes recycling nutrient and detoxifying ecosystems are capable to fulfil the future energy need by producing biohydrogen by due to the coupling of autotrophic and heterotrophic microbes. In granules microbes mutualy exchanging nutrients and electrons for hydrogen production. The consortial biohydrogen production depend upon constituent microbes, their interdependence, competition for resources, and other operating parameters while remediating a waste material in nature or bioreactor. The present review deals with development of granular algae-bacteria consortia, hydrogen yield in coculture, important enzymes and possible engineering for improved hydrogen production.

Introduction

Hydrogen (H) is the most abundant atom in the universe. Molecular hydrogen (H2) having high calorific value is non polluting carbon-free energy resource. The present sources of H2 such as, oil gas, gasification (Lv et al., 2019), advanced pyrolysis (Foong et al., 2021)), thermocatalysis of methane(Naikoo et al., 2021), electrolysis etc. are not fee from issue of environmental pollution. The biological H2 production is not only pollution free but also can assist remediation of pollutants from a range of habitas. Many photosynthetic microbes (bacteria, cyanobacteria, and micro-algae) grow on the waste effluents and produce H2 in both pure culture as well as in the co-culture conditions. Aerobic autotrophic H2 producer utilize electrons generated by photolysis of water in photosynthesis. They utilize light enegy for generating reducing power (ATP and NADPH2) for synthesizing food by reducing CO2. Light is not required the anaerobic H2 producing microbes. Potential microbes are continuously being updated for their biological H2 (Bio-H2) production (Kruse et al., 2018) as the rising demand for clean fuel H2 is likely to be fulfilled by synthetic or biological catalysts.

Production of bio-H2 is promising due to low cost, renewable and environmental friendly nature. The bio-H2 production systems based on the photo-heterotrophic combination generally uses lowcost or wastes substrates of industry or agricultural products, thus coupling waste treatment and bio-H2 production (Koók et al., 2016). In dark fermentation, organic compounds are converted to organic acids, CO2, alcohols and H2 by microbes (Calusinska et al., 2015). Metabolites of dark fermentation and other metabolites (glucose, sucrose and succinate) are transformed to H2, CO2 along with other by products anaerobically by photo-fermentative pathway in many green algae (Kim et al., 2014, Chandra and Venkata Mohan, 2011; Hwang et al., 2014; Boboescu et al., 2016). The production of bio-H2 utilize renewable resources or waste lignocellulosis materials of food / kitchen waste, agricultural waste, dairy waste etc. (Cheng et al., 2011, Goswami et al., 2021, Srivastava et al., 2021, Bhatia et al., 2021, Singh et al., 2021).

In natural habitats, microbes grow in association with a dynamically changing communities with time by developing syntrophic interdependence with each other in the functional ecosystem or the microbial consortia (biofilm and granules). A better understanding of microbial interrelation and interdependence can facilitate consortial management and proper engineering for obtaining desired value products or H2 production (Ergal et al., 2022). The pure culture study of microbe are useful for biotechnological experiments providing well defined experimental outcome, but compromizing the physiological and ecological boundaries of microbes in isolated state (Grandel et al., 2021). In contrast, the consortia growth of microbe facilitate their optimum bio-production potential by enabling their different eco-physiological functions, multitude of possible metabolic reaction and interaction possibilities. The streamlined syntrophic interaction efficiently utilises undefined substrates available in consortia, low product inhibition, better eco-biotechnological optimization, and high yield (Ergal et al., 2020). In natural, artificial and conortial ecosystems, all the microbe are not equally important in performing a desired function. Thus, for obtaining a specific product by efficient conversion of a substrate, only specific microbial species are more important compared to the species richness of the consortia (Cabrol et al., 2017).

Microbial constituents of aerobic and anaerobic granular consortia vary depending upon the environment where consortia develop. One constituent of the aerobic consortia are unicellular algae (such as Chlorella and Scenedesmus)with bacteria whereas in anaerobic consortia, anaerobic bacteria (such as Clostridium) are present (Liu et al., 2017, Zhang et al., 2008). In anaerobic granulation based treatment plants parameters like reactor operation, system performance, physicochemical factors and microbes have been reviewed along with bioreactor designs, for granulation while bio-H2 production and concomitant degradation of recalcitrant pollutants (Show et al., 2020). In aerobic consortia, physicochemical environment and constituent microbes differ from anaerobic system. There may be differences in initiation, development and maturation of anaerobic and aerobic granules, however there are common factors in both type of granule formation. The present review deals with development of granular algae-bacteria consortia, hydrogen yield in coculture, important enzymes and possible engineering for improving hydrogen production.

Section snippets

Process of granulation

Granule formation takes place in sequential manner involving quorum sensing and interaction of microbial cells, formation of micro-aggregates of microbial cells, synhesis of extracellular polysaccharide (EPS) by aggregated cells followed by maturation of granules under operation condition of reactor (Zhang et al., 2016). Time required for granulation time vary from two days to 90 days depending upon the type of waste (synthetic / real waste or effluents) used in the sequencial batch reactor (

Hydrogen production pathway

The microalgae C. reinhardtii is caable to produce H2 by switching from autotrophic mode to heterotrophic mode depending upon the nutrient availability and environmental condition. This algae produce H2 by linking the PSII and with direct biophotolysis of H2O. The three pathways for H2 production in this algae are depicted in Fig. 1.

Photobiological hydrogen (Photobio-H2) production

The photobio-H2 production in C. reinhardtii wild type cultures have four phases: first, an aerobic phase (accumulation of O2 and it consumption in respiration; second, a lag phase without evolution of O2 or H2 by the culture; third photobio-H2-production phase, and fourth, termination of photobio-H2 production (Kosourov et al., 2002). Hydrogen production in green algae is a physiological transitory biochemical pathway because co-production of O2 and H2 compete for accepting e generated in

Photo-fermentation

Purple non-sulfur photosynthetic (PNSP) bacteria are the best known non-oxygenic H2 producers. Some of the PNSP bacteria are Rhodopseudomonas palustris, Rhodospirillum rubrum, Rhodobacter sphaeroides and R. capsulatus that produce H2 with the help of N2-ases and the activity of production of H2 is similar to cyanobacteria. N2-ase uses the ATP produced in photosynhesis for the generation of H2, the source of e in these bacteria are organic acid instead of water and thus not evolve O2. The most

Dark fermentative hydrogen production

Besides photobio-H2, high rate, stable and sustainable dark fermentative hydrogen (DF-H2) could be produced using organic waste (Das and Veziroglu, 2001). Its production by use of granules are the most promising for treating organic waste and generating clean H2 energy. For enhancing H2 yield, immobilization, organic waste types, and supporting materials are important factors (Banu et al., 2018). Anaerobic mixed microflora of sewage sludge are good seed for DF-H2 production (Chang and Lin, 2004

Important enzymes in biological H2 production

In contrast to higher photosynthetic plants, many cyanobacteria and micro-algae have capability to rearrange the e and H+ for evolution of the H2. They contain enzyme H2ase and N2-ase that are central to the H2 production by microalgae and cyanobacteria.

Inter-dependence and co-operations among microbes in granule for H2 production

Absence of key element N and S promotes starch accumulation in the microalgae cell. The starch degradation through glycolysis will activate the H2 production by PSII independent pathway via plastoquinine or by PFR pathway(Baltz et al., 2014, Jans et al., 2008). Starch rich microalgae provide nutrient support to heterotrophs. There are reports regarding enhanced starch accumulation in the algae-bacteria co-culture, however there is no precise evidences in this regard. Variety of products are

Strategegies for improving H2 yield

H2 yield can be improved by adapting many startegegies depending upon the system used. If considering the cyanobacterial system inhibition of uptake hydrogenase(HupSL) could be a target(Lindblad, 2018). However, its inactivation may reprogramming may alter cell health and overall H2 production.(Kourpa et al., 2019). Alternatively the flow of electrons could be increased toward the this H2ase. The gene Flv3B expressing in heterocyst and eliminating O2 for N2 fixing activity. The over expression

Future perspective

Study of algal microbiome is new field with limited number of studies in reference to the algal phycosphere (Krohn-Molt et al., 2017), and even lower number of data are available regarding interaction with bacteria (Gonzalez and Bashan, 2000; Croft et al., 2006; Higgins et al., 2018). The basic understanding of such interactions with host algae will facilitae for better bioreactor design and improving growth with bacteria. The combined use of hybrid system are likely to fulfil duel role of waste

Conclusion

The biological H2 production using granular consortia of algae and bacteria is promising field of reaserch for the producing clean and sustainable H2 for the future. However, limited number of research data are available till date and findings are mainly based on the co-colture data. The field require more investigation precise assigning role of microbes in the granule. A better knowledge about coordinate use of resource in granule, use of metabolically engineering microbes in granule

CRediT authorship contribution statement

Deen Dayal Giri: Writing – original draft. Himanshu Dwivedi: Writing – original draft. Abdulmohsen Khalaf D. Alsukaibi: Conceptualization, Writing – original draft. Dan Bahadur Pal: Writing – original draft. Ahmed Al Otaibi: Writing – original draft. Mohammed Yahya Areeshi: Writing – original draft. Shafiul Haque: Writing – original draft. Vijai Kumar Gupta: Writing – review & editing, Supervision.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgement

The authors DDG and HD thankfully acknowledge MS College for institutional support. DBP acknowledge Birla Institute of Technology, Mesra, Ranchi, Jharkhand for institutional and financial support. VKG would like to acknowledge the institutional research funding supported by the SRUC, UK.

References (113)

  • N. Fakhimi et al.

    Improving hydrogen production using co-cultivation of bacteria with Chlamydomonas reinhardtii microalga

    Materials Science for Energy Technologies

    (2019)
  • S.Y. Foong et al.

    Progress in waste valorization using advanced pyrolysis techniques for hydrogen and gaseous fuel production

    Bioresour. Technol.

    (2021)
  • R.K. Goswami et al.

    Advanced microalgae-based renewable biohydrogen production systems: A review

    Bioresour. Technol.

    (2021)
  • N.E. Grandel et al.

    Control of synthetic microbial consortia in time, space, and composition

    Trends Microbiol.

    (2021)
  • J. He et al.

    Enhanced hydrogen production through co-cultivation of Chlamydomonas reinhardtii CC-503 and a facultative autotrophic sulfide-oxidizing bacterium under sulfurated conditions

    Int. J. Hydrogen Energy

    (2018)
  • Y.-S. Jang et al.

    Metabolic engineering of Clostridium acetobutylicum for butyric acid production with high butyric acid selectivity

    Metab. Eng.

    (2014)
  • L. Jiang et al.

    Butyric acid: Applications and recent advances in its bioproduction

    Biotechnol. Adv.

    (2018)
  • O. Kruse et al.

    Improved photobiological H2 production in engineered green algal cells

    The Journal of Biological Chemistry

    (2005)
  • W. Li et al.

    Enhanced biohydrogen production from sugarcane molasses by adding Ginkgo biloba leaves

    Bioresour. Technol.

    (2020)
  • J.-Z. Liu et al.

    Exogenic glucose as an electron donor for algal hydrogenases to promote hydrogen photoproduction by Chlorella pyrenoidosa

    Bioresour. Technol.

    (2019)
  • L. Liu et al.

    Development of algae-bacteria granular consortia in photo-sequencing batch reactor

    Bioresour. Technol.

    (2017)
  • L. Liu et al.

    Characteristics and performance of aerobic algae-bacteria granular consortia in a photo-sequencing batch reactor

    J. Hazard. Mater.

    (2018)
  • Q. Liu et al.

    Phosphate enhancing fermentative hydrogen production from substrate with municipal solid waste composting leachate as a nutrient

    Bioresour. Technol.

    (2015)
  • J. Lv et al.

    Steam co-gasification of different ratios of spirit-based distillers’ grains and anthracite coal to produce hydrogen-rich gas

    Bioresour. Technol.

    (2019)
  • W. Ma et al.

    Treatment with NaHSO3 greatly enhances photobiological H2 production in the green alga Chlamydomonas reinhardtii

    Bioresour. Technol.

    (2011)
  • J. Manoyan et al.

    Regulation of biohydrogen production by protonophores in novel green microalgae Parachlorella kessleri

    J. Photochem. Photobiol., B

    (2019)
  • E. Mignolet et al.

    Function of the chloroplastic NAD(P)H dehydrogenase Nda2 for H₂ photoproduction in sulphur-deprived Chlamydomonas reinhardtii

    J. Biotechnol.

    (2012)
  • F. Mus et al.

    Inhibitor studies on non-photochemical plastoquinone reduction and H(2) photoproduction in Chlamydomonas reinhardtii

    BBA

    (2005)
  • J. Noth et al.

    Pyruvate:ferredoxin oxidoreductase is coupled to light-independent hydrogen production in Chlamydomonas reinhardtii

    J. Biological Chem.

    (2013)
  • Y.-K. Oh et al.

    Current status of the metabolic engineering of microorganisms for biohydrogen production

    Bioresour. Technol.

    (2011)
  • E.A. Peden et al.

    Identification of global ferredoxin interaction networks in Chlamydomonas reinhardtii

    J. Biological Chem.

    (2013)
  • D. Petroutsos et al.

    PGRL1 participates in iron-induced remodeling of the photosynthetic apparatus and in energy metabolism in Chlamydomonas reinhardtii

    J. Biological Chem.

    (2009)
  • M. Renaudie et al.

    Biohydrogen production in a continuous liquid/gas hollow fiber membrane bioreactor: Efficient retention of hydrogen producing bacteria via granule and biofilm formation

    Bioresour. Technol.

    (2021)
  • S.J. Sarma et al.

    Finding Knowledge Gaps in Aerobic Granulation Technology

    Trends Biotechnol.

    (2017)
  • O. Schmitz et al.

    HoxE–a subunit specific for the pentameric bidirectional hydrogenase complex (HoxEFUYH) of cyanobacteria

    BBA

    (2002)
  • K.-Y. Show et al.

    Anaerobic granulation: A review of granulation hypotheses, bioreactor designs and emerging green applications

    Bioresour. Technol.

    (2020)
  • T. Singh et al.

    Integrated biohydrogen production via lignocellulosic waste: Opportunity, challenges & future prospects

    Bioresour. Technol.

    (2021)
  • N. Srivastava et al.

    Biohydrogen production using kitchen waste as the potential substrate: A sustainable approach

    Chemosphere

    (2021)
  • S.R. Subashchandrabose et al.

    Consortia of cyanobacteria/microalgae and bacteria: Biotechnological potential

    Biotechnol. Adv.

    (2011)
  • S.R. Vargas et al.

    do C. Chlamydomonas strains respond differently to photoproduction of hydrogen and by-products and nutrient uptake in sulfur-deprived cultures

    J. Environ. Chem. Eng.

    (2021)
  • T.K. Antal et al.

    Production of H2 by sulphur-deprived cells of the unicellular cyanobacteria Gloeocapsa alpicola and Synechocystis sp. PCC 6803 during dark incubation with methane or at various extracellular pH

    J. Appl. Microbiol.

    (2005)
  • A. Baltz et al.

    Plastidial expression of Type II NAD(P)H dehydrogenase increases the reducing state of plastoquinones and hydrogen photoproduction rate by the indirect pathway in chlamydomonas reinhardtii1

    Plant Physiol.

    (2014)
  • B.M. Barney

    Aerobic nitrogen-fixing bacteria for hydrogen and ammonium production: Current state and perspectives

    Appl. Microbiol. Biotechnol.

    (2020)
  • D.A. Betancourt et al.

    Characterization of diazotrophs containing Mo-independent nitrogenases, isolated from diverse natural environments

    Appl. Environ. Microbiol.

    (2008)
  • G. Boison et al.

    Transcriptional analysis of hydrogenase genes in the Cyanobacteria Anacystis nidulans and Anabaena variabilis monitored by RT-PCR

    Curr. Microbiol.

    (2000)
  • G. Boison et al.

    The rice field cyanobacteria Anabaena azotica and Anabaena sp. CH1 express vanadium-dependent nitrogenase

    Arch. Microbiol.

    (2006)
  • H. Bothe et al.

    Nitrogen fixation and hydrogen metabolism in cyanobacteria

    Microbiol. Mol. Biol. Rev.

    (2010)
  • L. Cabrol et al.

    Microbial ecology of fermentative hydrogen producing bioprocesses: Useful insights for driving the ecosystem function

    FEMS Microbiol. Rev.

    (2017)
  • C. Catalanotti et al.

    Fermentation metabolism and its evolution in algae

    Front. Plant Sci.

    (2013)
  • F.Y. Chang et al.

    Calcium effect on fermentative hydrogen production in an anaerobic up-flow sludge blanket system

    Water Science and Technology: A Journal of the International Association on Water Pollution Research

    (2006)
  • Cited by (16)

    View all citing articles on Scopus
    1

    These have equal contribution.

    View full text