Elsevier

Bioresource Technology

Volume 219, November 2016, Pages 72-79
Bioresource Technology

Improved biomass productivity in algal biofilms through synergistic interactions between photon flux density and carbon dioxide concentration

https://doi.org/10.1016/j.biortech.2016.06.129Get rights and content

Highlights

  • At a PFD of 100 μmol/m2/s inorganic carbon limitations occur below 2% CO2.

  • There is an interaction effect between CO2 and PFD on algae biofilm growth.

  • The model predicts optimal growth conditions to be 7.1% CO2 and 440 μmol/m2/s PFD.

  • The model predicted maximal biomass productivities of 4.4 g/m2/d, respectively.

  • Increasing growth parameters beyond their optimal ranges adversely affected growth.

Abstract

Algal biofilms were grown to investigate the interaction effects of bulk medium CO2 concentration and photon flux density (PFD) on biomass productivities. When increasing the CO2 concentration from 0.04% to 2%, while maintaining a PFD of 100 μmol/m2/s, biomass productivities increased from ∼0.5 to 2.0 g/m2/d; however, the productivities plateaued when CO2 concentrations were incrementally increased above 2–12%. Statistical analysis demonstrates that there is a significant interaction between PFD and CO2 concentrations on biomass productivities. By simultaneously increasing PFD and CO2 concentrations, biomass productivities were significantly increased to 4.0 and 4.1 g/m2/d in the experimental and modeled data, respectively. The second order model predicted increases in biomass productivities as both PFD and CO2 simultaneously increased yielding an optimum at 440 μmol/m2/s and 7.1%; however, when conditions were extended to the highest end of their respective ranges, the conditions were detrimental to growth and productivities decreased.

Introduction

Over the past several decades, researchers around the world have been studying algal growth systems to produce renewable bioresources such as bioenergy, bioplastics, fish and farm feed, nutraceuticals and pharmaceuticals. Algae are an attractive feedstock for these bioresources because they grow rapidly compared to most organisms, and the biomass has high concentrations of valuable biocompounds such as lipids/fatty acids and proteins; therefore, overall productivity of these biocompounds can be extraordinarily high under ideal growth conditions (Chisti, 2007). Currently, however, algal growth systems are not commercially viable for the production of most of these bioresources. There are several reasons for this, but perhaps the most significant is the high cost of harvesting and de-watering algal biomass grown planktonically. As such, several groups of researchers are focusing on growing algae as a biofilm, rather than a suspension culture. These algal biofilms offer potential harvesting and de-watering advantages because the algal biomass is: 1) immobilized, rendering it easily harvestable with novel reactor designs; 2) highly concentrated – up to 100 times more concentrated than planktonic growth systems (Christenson and Sims, 2012) – thus requiring less energy for de-watering the biomass before processing. Before algal biofilm growth systems can be scaled-up to industrial capacity, however, optimal conditions for growth must be established.

As with planktonic algal growth systems, carbon dioxide (CO2) concentration is an important factor in controlling the productivity of algal biofilm growth systems. In planktonic systems, significant increases in growth rates with increased dissolved CO2 concentrations have been observed, up until a threshold is reached where no further growth rate increase was observed (Chinnasamy et al., 2009, De Morais and Costa, 2007; Yun et al., 1996). In fact, these same studies demonstrated that very high concentrations of CO2 can become detrimental to growth. In contrast, studies of the effect of CO2 concentration on algal biofilm productivities have produced conflicting results. For instance, Blanken et al. (2014) reported very significant increases in algal biofilm growth rates when increasing the concentrations of inorganic carbon in the growth systems. However, Gross et al. (2013) and Kessano et al. (2015), reported no increases in algal biofilm growth rates when increasing the exposure concentrations of inorganic carbon. The reasons for the apparent contradictions across various biofilm systems are unknown but these differences perhaps betray an underlying and unappreciated complexity. Furthermore, algal biofilms do not necessarily respond to changes in environmental parameters in the same manner and magnitude that suspension cultures do (e.g. Schnurr et al., 2013 in the case of nitrogen stress). Thus, there is a need for a detailed characterization of algal biofilm growth responses to changing environmental parameters.

Under any given environmental condition, photosynthesis requires balanced light absorption by photosystem II and photosystem I to provide a consistent supply of ATP and NADPH, in the appropriate ratio, to support optimal rates of algal CO2 fixation and growth. Dynamic fluctuations in light and CO2 concentration affect the photosynthesis rate and evoke acclimation responses from algal cells that readjust the balance between light harvesting complexes and the CO2 fixation system over short and long term time scales (Huner et al., 1998, Falkowski and Raven, 2007). For example, excess excitation energy (light) may lead to photo-oxidative damage to the photosynthetic apparatus, short-term photo-inhibition of CO2 fixation and slower growth (Huner et al., 1998, Takahashi and Murata, 2008); however, these effects are mitigated through dissipation of excess excitation energy by non-photochemical quenching mechanisms, the xanthophyll cycle in eukaryotic algae (Jahns and Holzwarth, 2012), photosystem II repair mechanisms (Takahashi and Murata, 2008, Nixon et al., 2010, Järvi et al., 2015) and/or the use of alternative electron acceptors beyond CO2. Increasing CO2 will also dissipate excess electrons by increasing rate of photosynthetic carbon reduction if intermediates of the cycle (i.e., ribulose, 1–5, bisphosphate) are available and sufficient to support increased activity. Enhanced CO2 supply may arise from abiotic as well as biotic factors such as increased bacterial respiration or induction of an algal CO2 concentrating mechanism, which permits superior utilization of existing CO2 resources while at the same time using the excess light to energize the system (de Araujo et al., 2011, Wang et al., 2011). In contrast to planktonic algae, algal biofilms present a unique environment where the effect of CO2-photon flux density (PFD) interaction is amplified over small distances due to the concentrated nature of the biomass that rapidly attenuates both light and CO2, disturbing the photosynthetic balance. The interactive effects of light and CO2 on algal biofilm growth have been modeled mathematically using a variety of approaches, which indicate a very complex relationship with respect to growth. Light-limitation frequently is the determining factor in algal biofilm growth while CO2 limitation becomes more acute as the thickness of the biofilm increases (Liehr et al., 1990, Flora et al., 1995). Few studies, however, have experimentally assessed the direct response of algal biofilm growth rates in response to co-varying light and CO2 with the purpose to identify interaction effects, which we address here.

In this study, two hypotheses were tested: 1) algal biofilm growth rates will increase as dissolved carbon dioxide concentrations are increased in the growth medium until a threshold is met; 2) there is an interaction effect of PFD and CO2 concentration on algal biofilm growth kinetics. The objectives of this paper, therefore, were to study the effects of CO2 concentrations on algal biofilm growth kinetics from a one-variable-at-a-time approach i.e. only CO2 concentration is changed between experiments, and to study the interaction effects of CO2 concentration and PFD on algal biofilm growth kinetics.

Section snippets

Flat-plate parallel horizontal algae biofilm culturing systems

Two similarly designed semi-continuous flat plate parallel, horizontal photobioreactors (PBR) were used in this study. System #1 (Schnurr et al., 2013) was comprised of 18 glass growth coupons (Fig. 1), each housed in a separate compartment, with separate inlet and outlet flow ports for the circulation of growth media. System # 2 was comprised of a common housing containing 24 polycarbonate growth coupons (Fig. 2). Circulation of growth medium through the housing occurred via a single inlet and

The effect of carbon dioxide concentration on algal biofilm growth kinetics

Algal biofilm biomass productivities significantly increased with increasing CO2 concentration until a threshold was met and growth rates plateaued (Fig. 4). Linear regression analysis of algal biomass data collected over 26 day growth periods (Fig. S1) showed significant increases in overall productivities when CO2 concentrations were increased from atmospheric (0.04%) to 2% (v/v). When CO2 concentrations were increased beyond 2% up to 12%, no further increase in biomass productivities was

Conclusions

The results from this paper demonstrate that bulk medium CO2 concentrations and the interacting effects of PFDs and CO2 concentrations have significant affects on algae biofilm biomass productivities. At a fixed PFD of 100 μmol/m2/s, algae biofilm biomass productivities were significantly increased from ∼0.5 to 2 g/m2/d as CO2 concentrations were increased from atmospheric to 2%. Incrementally increasing CO2 concentrations from 2% to 12%, however, caused no statistical difference in algae biofilm

Acknowledgements

The authors would like to thank the Natural Science and Engineering Research Council of Canada (NSERC) for financial support in the form of a Strategic Grant (#STPGP 463037 – 2014), a Canadian Graduate Scholarship (CGS D) (P.J.S.), and a Postgraduate Scholarship (PGS D) (O.M.). Additional thanks to HATCH Ltd. for financial support in the form of a Graduate Student Scholarship for Sustainable Energy Research. Lastly, special acknowledgement and thanks to Pond Biofuels Inc. for helping develop

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