ReviewSustainable production of algae-bacteria granular consortia based biological hydrogen: New insights
Graphical abstract
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.
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