Phototrophic Biofilms and Their Potential Applications
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View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Springer - Publisher Connector J Appl Phycol (2008) 20:227–235 DOI 10.1007/s10811-007-9223-2 Phototrophic biofilms and their potential applications G. Roeselers & M. C. M. van Loosdrecht & G. Muyzer Received: 23 February 2007 /Revised and Accepted: 19 June 2007 /Published online: 12 August 2007 # Springer Science + Business Media B.V. 2007 Abstract Phototrophic biofilms occur on surfaces exposed The photosynthetic activity fuels processes and conver- to light in a range of terrestrial and aquatic environments. sions in the total biofilm community. For example, Oxygenic phototrophs like diatoms, green algae, and heterotrophs derive their organic C and N requirements cyanobacteria are the major primary producers that generate from excreted photosynthates and cell lysates, while energy and reduce carbon dioxide, providing the system nutrient regeneration is enhanced by heterotrophs (Bateson with organic substrates and oxygen. Photosynthesis fuels and Ward 1988). processes and conversions in the total biofilm community, The microorganisms produce extracellular polymeric including the metabolism of heterotrophic organisms. A substances (EPS) that hold the biofilm together (Flemming matrix of polymeric substances secreted by phototrophs and 1993; Wimpenny et al. 2000). Thick laminated multilayered heterotrophs enhances the attachment of the biofilm phototrophic biofilms are usually referred to as microbial community. This review discusses the actual and potential mats or phototrophic mats (Guerrero et al. 2002; Roeselers applications of phototrophic biofilms in wastewater treat- et al. 2007a; Stal et al. 1985; Ward et al. 1998). The top ment, bioremediation, fish-feed production, biohydrogen layer of microbial mats is typically dominated by oxygenic production, and soil improvement. phototrophs, such as cyanobacteria (Castenholz 2001a) and diatoms, with underlying or intermixed layers of anoxy- Keywords Algae . Cyanobacteria . Microbial mats . genic phototrophs, i.e. green and purple sulfur bacteria Periphyton . Photosynthesis . Bioremediation (GSB and PSB) (Martinez-Alonso et al. 2005)and Chloroflexi like bacteria (Castenholz 2001b; Ruffroberts et al. 1994). Introduction Steep vertical redox and chemical gradients (∼microns to millimeters) that establish in phototrophic biofilms and Phototrophic biofilms can best be described as surface mats enforce these stratifications in the microbial commu- attached microbial communities driven by light energy with nity (Fig. 1). a photosynthesizing component clearly present. Oxygenic Light intensity decreases with depth, restricting photo- phototrophic microorganisms such as benthic diatoms trophic activity to the upper layer of the mat. Oxygenic (centric, pennate, unicellular, and filamentous), unicellular photosynthesis results in a steep oxygen gradient that and filamentous cyanobacteria, and benthic green algae restricts most anoxygenic phototrophs and anaerobic generate energy and reduce carbon dioxide, providing chemotrophs to the lower parts of the mat. However, recent organic substrates and oxygen. studies have also shown examples of anaerobes thriving in the oxic zone of microbial mats (Cypionka 2000; Schaub : : and Van Gemerden 1994). The utilization of CO2 during G. Roeselers M. C. M. v. Loosdrecht G. Muyzer (*) photosynthesis results in a pH gradient (Revsbech et al. Department of Biotechnology, Delft University of Technology, 1983). Julianalaan 67, 2628 BC Delft, The Netherlands Phototrophic biofilms and mats are formed on surfaces e-mail: [email protected] in a range of terrestrial and aquatic environments (Chan 228 J Appl Phycol (2008) 20:227–235 Cyanobacteria can assimilate nitrogenous compounds like ammonium, nitrate, nitrite, urea, and amino acids. Diazotrophic cyanobacteria can also assimilate atmospheric nitrogen (N2) (Flores and Herrero 2005). However, the reduction of dinitrogen gas to ammonia by nitrogenases is a highly endergonic reaction requiring metabolic energy in the form of ATP. Protection of the sensitive enzyme complex from inactivation by O2, and the replacement of the damaged enzyme add to this high metabolic cost. The capability of nutrient removal in the absence of organic carbon has often been used for wastewater treatment in algal pond systems (Davis et al. 1990; Garcia et al. 2000). A major disadvantage using suspended algae is the high secondary organic pollution caused by algae Fig. 1 This cross section reveals the stratified structure of a thick biomass in the effluent of the ponds (Racault 1993). freshwater phototrophic biofilm. The dark top layer consists predom- Biomass can be removed by filtration, sedimentation with inantly of Oscillatoria like cyanobacteria. Scale bar indicates 1 mm centrifugation, or with decantation, but most of these methods are costly. By using immobilized phototrophic et al. 2003; Ferris et al. 1997; Ortega-Morales et al. 2000). biofilms the problem of separation of suspended algal The oldest fossilized phototrophic biofilm or mat-like biomass and water can be avoided and the nitrogenous structures date back approximately 3.5 billion years compounds retained in algal biomass can be harvested and (Des Marais 1990). used as fertilizers in agriculture (Schumacher and Sekoulov Currently, there is a growing interest in the application of 2002). phototrophic biofilms, for instance, in wastewater treatment An interesting feature of some cyanobacteria is that they (Craig et al. 1996; Schumacher and Sekoulov 2002; can accumulate inorganic phosphorus and store it internally Vymazal et al. 2001), bioremediation (Blanco et al. 1999; as polyphosphates (Kromkamp 1987). However, this aspect Chaillan et al. 2006; Cohen 2002), aquaculture (Bender and has hardly been explored in the context of wastewater Phillips 2004; Phillips et al. 1994, van Dam et al. 2002), treatment. and biohydrogen production (Prince and Kheshgi 2005; The photosynthetic activity in phototrophic biofilms Tsygankov et al. 1999). The present review will give a brief results in an increasing pH due to the change of the carbon introduction to various actual and potential biotechnologi- dioxide equilibrium in water. This increase in pH causes cal applications of phototrophic biofilms. precipitation of dissolved phosphates, in addition to phosphorus removal by assimilation. This photosynthesis induced pH increase has also shown potential for the Wastewater treatment reduction of faecal coliform bacteria in wastewater streams (Schumacher et al. 2003). The application of oxygenic phototrophs in the treatment of European Union regulations have led to more stringent waste streams that are relatively rich in nutrients and low in effluent standards for sewage treatment facilities located in organic carbon has many advantages. In a heterotrophic ecologically sensitive areas. Phototrophic biofilms can be biofilm O2 transfer by diffusion is limited to approximately applied for the additional nutrient removal from secondary − − 20 nmol cm 2 min 1. However, the areal net oxygen effluents of wastewater treatment plants. Nutrient removal production in an active phototrophic biofilm at a light in so-called constructed wetlands (Fig. 2), which show − − intensity of 1,000 μmol photons m 2 s 1 is approximately a potential for small-scale wastewater treatment, depends also factor of two higher (Epping and Kuhl 2000). Hence, the to a large extent on the activity of epiphytic phototrophic oxygen that is produced by phototrophs can cover a great biofilms growing on reed stems (Larsen and Greenway part of the oxygen demand of bacterial nitrification and the 2004; Ragusa et al. 2004). Table 1 shows the nitrogen and heterotrophic consumption of organic carbon. In adition, phosphorus removal rates obtained with several photo- oxygenic phototrophs assimilate nutrients for building trophic biofilm-based wastewater polishing systems. biomass with carbon dioxide as carbon source. In contrast For process control and system optimization, it is to wastewater treatment by bacterial nitrification and important to define the right operational conditions. Craggs denitrification, where a large part of the nitrogen escapes et al. (1996) described several parameters that determine the as N2 gas to the atmosphere, the nitrogenous compounds efficiency of nutrient removal in an experimental photo- are in this case retained in algal biomass. trophic biofilm system. An important parameter is the J Appl Phycol (2008) 20:227–235 229 walls. These “passive” mechanisms can take place at the cellular level and at the microbial community level. The active mode of metal uptake and concentration is called bioaccumulation. This process is dependent on the cellular metabolism. Many oxygenic phototrophic microorganisms have the capability to sorb or accumulate metals in one way or another, and there is considerable potential for the applica- tion of algal biofilms in the detoxification of wastewaters polluted with heavy metals (Bender et al. 1994; Mehta and Gaur 2005). Extracellular polysaccharides that are nega- tively charged at elevated pH levels generated by oxygenic photosynthesis may account for the metal-binding proper- ties of phototrophic biofilms (Bender et al. 1994; Bhaskar and Bhosle 2006; Liu et al. 2001; Wang et al. 1998). Parker et al. (2000) showed that mucilage sheaths isolated from the cyanobacteria Microcystis aeruginosa and Aphanothece halophytica exhibit strong affinity for heavy metal ions such as copper, lead,