Microbial technology with major potentials for the urgent environmental needs of the next decades.

Several needs in the context of the water-energy-food nexus will become more prominent in the next decades. It is crucial to delineate these challenges and to find opportunities for innovative microbial technologies in the framework of sustainability and climate change. Here, we focus on four key issues, that is the imbalance in the nitrogen cycle, the diffuse emission of methane, the necessity for carbon capture and the deterioration of freshwater reserves. We suggest a set of microbial technologies to deal with each of these issues, such as (i) the production of microbial protein as food and feed, (ii) the control of methanogenic archaea and better use of methanotrophic consortia, (iii) the avoidance of nitrification and (iv) the upgrading of CO2 to microbial bioproducts. The central message is that instead of using crude methods to exploit microorganisms for degradations, the potentials of the microbiomes should be used to create processes and products that fit the demands of the cyclic market economy.

Introduction

In our current society, we must deal with numerous issues to sustain or even improve the general quality of life of the 7 billion people that currenpan>tly inpan>habit the earth. The pan> class="Chemical">water–energy–food nexus can be considered one of these key issues for the coming decades (Walker et al., 2014). The lingering anticipated climate change adds a fourth factor to this nexus (Beck and Walker, 2013), which makes it more complicated to find suitable solutions that cover multiple aspects.

The development and optimization of environmental microbial technologies over the last century led to multiple applications in this framework. To decrease the pollution from municipalities and industries, the activated sludge process was developed over a cenpan>tury ago (Ardern anpan>d Lockett, 1914). Continpan>uous inpan>novation has allowed this process to shift from a mere wastepan> class="Chemical">water clean‐up technology to a provider of renewable energy (Verstraete and Vlaeminck, 2011; De Vrieze et al., 2016). Anaerobic digestion of the collected organics hosts a central position in the current wastewater treatment approach, as it serves as the provider of renewable energy. Depending on the process conditions, it also enables the recovery of nutrients and/or organics (Holm‐Nielsen et al., 2009; Batstone and Virdis, 2014). Of crucial importance in this context is the evolution of the world energy prices. Currently, energy prices are low, amongst others due to the breakthroughs in the fracking technology, although the long‐term sustainability of this process is highly questionable (Inman, 2014; IEA, 2016). Future energy prices are predicted with a high degree of uncertainty, amongst others due to the major advances in photovoltaic and wind technologies (Cabrera‐Tobar et al., 2016).

It appears that for the future wastewater treatmenpan>t, the production of biogas should no longer be directed to enpan>ergy recovery, rather biogas anpan>d the nutrienpan>ts presenpan>t inpan> wastepan> class="Chemical">water must be tuned for reuse by upgrading them into valuable molecules (Cagnetta et al., 2016). The recent advances in single cell protein production, which is the production of protein‐rich feed and food, using recovered nutrients and organics, open possibilities for new microbial technological applications to short‐circuit nutrient and energy cycles into more efficient processes (Matassa et al., 2015). The combination of wastewater treatment and single cell protein production technologies possesses the potential to substantially influence the water–energy–food–climate nexus of the coming decades.

The application of microbial potentialities highlights the emergence of other issues that are directly or indirectly related. We focused on the major challenges of the coming decade, in relation to climate change and sustainability, and the microbial technologies that can be applied to tackle them (Fig. 1).

Figure 1

Schematic overview of specific global threats of the coming decades and concomitant potential microbial solutions.

The urgent needs

The planetary boundary conditions: nitrogen is also an issue

The discovery of the Haber–Bosch process for nitrogen fixation inpan> the beginpan>ninpan>g of the 20th cenpan>tury has beenpan> one of the mainpan> drivers behinpan>d the global population expanpan>sion sinpan>ce 1950 (Erismanpan> et al., 2008). Anpan> importanpan>t fraction of this pan> class="Chemical">reactive nitrogen ends up in the surface waters, which leads to the reactive nitrogen flow strongly surpassing the planetary boundaries, with a high risk of destabilization of the earth ecosystem (Steffen et al., 2015). The nitrification process leads to massive losses of reactive nitrogen in various natural and manmade ecosystems, caused by both washout from the soil and denitrification to N2 (Subbarao et al., 2006). Time has come to focus on controlling nitrification, for instance by implementing a new generation of slow‐release fertilizers and, if possible, plant‐generated nitrification inhibitors (O'Sullivan et al., 2016). A similar approach should be applied in wastewater treatment in which nitrogen recovery, rather than dissipation via the nitrification/denitrification process should be targeted. Nitrification should be labelled as an environmentally undesirable process, and major efforts should be undertaken to avoid it. The need to recover/reuse the nitrogen present in our secondary resources does not originate from a source deficiency, unlike certain rare earth elements (Hennebel et al., 2015), but from a sink overload. Dealing in a drastically different way with nitrogen relates with the optimal use of fossil energy and preservation of the environmental quality.

At present, 1–2% of the energy consumption on earth is used to fuel the Haber–Bosch process for nitrogen fixation. Yet, depenpan>dinpan>g on the pan> class="Species">human diet (vegetarian or carnivorous), only 4–16% of this nitrogen is consumed (Galloway and Cowling, 2002; Matassa et al., 2015). To sustain the food (nitrogen) supply to the growing world population, soy production has boomed over the last two decades (Dalin et al., 2012), with an increase from 17 million tons in 1960 to 230 million tons in 2008 (Hartman et al., 2011). The growing risk of irreversible deforestation and the fact that the production of soya bean coincides with 0.3–0.6 kg CO2 equivalents per kg of fresh weight do not support a sustainable expansion of this potential and imply the need for alternative nitrogen sources to be used as feed or food (Dalin et al., 2012; Castanheira and Freire, 2013). An alternative solution lies in the production of single cell proteins, also called microbial proteins. These do not compete for land usage with other crops, and much higher nitrogen efficiencies can be obtained, especially when used directly as food source (Matassa et al., 2015; Pikaar et al., 2017). The key aspect of microbial protein production for feed and food lies in the ability to use recovered nitrogen from different sources, such as source‐separated urine (Maurer et al., 2003; Luther et al., 2015) and the liquid fraction of digestate (Desloover et al., 2012). This has multiple advantages, as it (i) avoids additional costs for reactive nitrogen conversion to nitrogen gas, (ii) decreases the amount of nitrogen to be fixed by Haber‐Bosch and (iii) prevents excessive accumulation of reactive nitrogen in the biosphere.

Climate change: the diffuse methane emissions and their abatement

Anaerobic digestion provides the possibility to stabilize organic waste streams, which results in the controlled production of CH4‐rich biogas. This biogas canpan> be (i) used for flexible electricity anpan>d heat production (Szarka et al., 2013), (ii) upgraded to biopan> class="Chemical">methane for injection on the smart gas grid (Lund et al., 2012; Junne and Kabisch, 2017) or (iii) used as carbon source for microbial feed and food production (Strong et al., 2015). Part of the methane, however, remains dissolved in the effluent or digestate (Cakir and Stenstrom, 2005; Liebetrau et al., 2010). For low‐strength wastewaters, this can easily exceed 25% (Hartley and Lant, 2006), which reflects a simultaneous high loss in energy recovery potential and emission of a potent greenhouse gas to the atmosphere, as it has a global warming potential of 28 CO2 equivalents (Saunois et al., 2016). Other engineered or natural anaerobic microbial ecosystems, such as septic tanks, manure pits, landfills, sewers, activated sludge, rice paddies, wetlands and particularly the methanogens active in ruminants also contribute to the diffuse release of methane (Johnson et al., 2007; Perez‐Barberia, 2017). The diversity of sources of diffuse methane emissions implies the need for case‐specific solutions.

The dissolved methane, oftenpan> at supersaturation (Hartley anpan>d Lanpan>t, 2006), inpan> the liquid effluenpan>t of anpan>aerobic digesters canpan> be mitigated, for example, via the methalgae approach (pan> class="Disease">van der Ha et al., 2011). Methanogenesis in the rumen can be inhibited by adding, for example, 3‐nitrooxypropanol to the feed (Romero‐Perez et al., 2014; Duin et al., 2016) or by applying antibodies to prevent adhesion of Methanobrevibacter (Ng et al., 2016). However, methanogenesis might be essential for cellulose digestion in the rumen (Mason and Stuckey, 2016), which accentuates the need to look for other routes than ruminants to supply high‐quality proteinaceous foods. Methane emission from wetlands or rice paddies can be decreased by short‐term drainage or temporary oxygen supply (Ratering and Conrad, 1998; Arends et al., 2014). Methane emissions from lakes can be controlled by steering aquatic trophic interactions to minimize grazing of methanotrophs by zooplankton (Devlin et al., 2015). This demonstrates that there is huge potential of challenging microbial engineering systems to deal with diffuse methane emissions and their impact on climate change.

Microbial biotechnology for CO2 capture

The atmospheric CO2 concenpan>tration has beenpan> inpan>creasinpan>g sinpan>ce the mid‐18th cenpan>tury inpan> response to pan> class="Species">human activities (Menon et al., 2007). To reduce global CO2 emissions to 80% of the levels of 1990 by 2050, we need to achieve a 4200 Mt CO2 sequestration per year (Mac Dowell et al., 2017). To deal with this challenge, we rely on carbon capture and storage (CCS) and carbon capture and utilization (CCU). The overall perspective of the chemical conversion of CO2 to organic compounds, such as urea and methanol, is estimated to contribute only 1% to the necessary CO2 reduction requirement (Mac Dowell et al., 2017). This emphasizes the need to consider alternative options, amongst which microbial processes to contribute to CO2 sequestration deserve to be explored. The soil microbial ecosystem, as well as the ocean ecosystem, has been important sinks for CO2, which partially mitigated the human impact on the carbon cycle (Menon et al., 2007). The importance of the soil microbial community in the sequestration of carbon suggests that there is a huge potential to maximize CO2 sequestration through microbial community engineering.

A change in land use from arable land to grassland entails an average 18% higher carbon sequestration, which relates with a yearly pan> class="Chemical">carbon input of 0.75 tonnes C ha−1 year−1 (Kampf et al., 2016). A soil with a limited degree of manipulation reaches a higher degree of microbial homoeostasis (Cleveland and Liptzin, 2007), which allows a more efficient carbon sequestration. This type of soil management can be of great value in the context of the anticipated climate change (Fontaine and Barot, 2005; Manzoni et al., 2012). An alternative approach lies in the addition of charcoal or biochar to the soil, which (i) is a direct addition of long‐term stable carbon to the soil, (ii) improves the overall soil quality and (iii) can adsorb nutrients to increase their plant bioavailability (Lehmann et al., 2006; Laird, 2008; Prost et al., 2013).

The concept of carbon sequestration canpan> also be approached by usinpan>g concenpan>trated pan> class="Chemical">CO2 sources. Microbial electrosynthesis allows the generation of valuable products from electricity, using CO2 or other organic feedstocks as carbon source (Nevin et al., 2010; Rabaey and Rozendal, 2010; Lovley, 2011). This enables the production of acetate (Gildemyn et al., 2015), butyrate (Ganigue et al., 2015) and other commodity chemicals (Nevin et al., 2011; Arends et al., 2017). These chemicals, when subjected to the process of microbial chain elongation, can be converted to medium chain fatty acids with a higher economic value, such as caproate and caprylate, which serve as bio‐based building blocks for the chemical industry (Agler et al., 2012; Spirito et al., 2014; Angenent et al., 2016). A key point in this process remains the energy‐efficient harvesting of these chemicals to obtain a concentrated stream with high product quality (Agler et al., 2011; Gildemyn et al., 2015; Andersen et al., 2016).

The ongoing deterioration of freshwater reserves

The intensive usage of nutrients, mainly N and P, results in at least a fraction of these nutrients ending up in the natural water bodies, which may result inpan> eutrophication (Conley et al., 2009; Coppenpan>s et al., 2016). The anpan>ticipated inpan>crease inpan> the pan> class="Species">human population is predicted to result in further eutrophication of terrestrial, freshwater and nearshore marine ecosystems (Tilman et al., 2001). Micropollutants are often insufficiently removed and accumulate in increasing amounts and even more staggering diversity in the surface waters (Margot et al., 2015). Although through river bank filtration > 90% of micropollutants can be removed in a period of 4 years, certain micropollutants show persistent behaviour, which may have a long‐term impact on the surface water biological quality (Hamann et al., 2016). This also directly affects our drinking water reserves (ground‐ and surface water), although drinking water production technologies are adequate to remove most micropollutants (Luo et al., 2014). However, this does not necessary result in a prompt change in suitable regulations (Sedlak, 2016). The main issue lies in the extent of removal, implying that future technologies need to deal with concentrations down to 1 μg l−1. These can be a combination of physical processes, for example increasing the concentrations by membrane technologies, and the use of the versatile bioconversion potential of naturally selected microbiomes.

The potential impact of persistent micropollutants implies the need for end‐of‐pipe treatment technologies in wastewater treatmenpan>t planpan>ts to safeguard the aquatic ecosystems. Biological treatmenpan>t canpan> be a suitable approach to remove micropollutanpan>ts from pan> class="Chemical">drinking water, but often requires bioaugmentation of suitable strains to be effective (Benner et al., 2013). A potential opportunity is the application of ammonium oxidizing bacteria that can co‐metabolize certain micropollutants down to the μg l−1 level (Kassotaki et al., 2016). Methane‐oxidizing communities can also be used for this purpose (Benner et al., 2015). Technologies combining physical concentration and advanced microbial physiology to deal with the enormous diversity of micropollutants still have a long way to go to safeguard our drinking and process water quality.

Cooperating with microorganisms

The crucial role of microorganisms in tackling the abovementioned challenges of the coming decades is apparent. To engage in more energy‐efficient processes with higher removal rates and efficiencies, we need to be able to control the microorganisms via an integrated approach. The way to go is to consider the microbial community as a structured three‐dimensionally organized entity, as used in the microbial resource management (MRM) (Marzorati et al., 2008; Read et al., 2011) and mixed culture biotechnology (Kleerebezem and van Loosdrecht, 2007) approaches. This also counpan>ts for the fields of pan> class="Species">human health and food safety, as total elimination of evolving microbial communities, rather than collaborating with them, leads to multiple side issues, such as antibiotic resistance (Baquero et al., 2008; Berendonk et al., 2015). An excellent example to avoid the usage of antibiotics is the biofloc technology as applied in aquaculture (Crab et al., 2012). Overall, a better understanding of the basics of the microbial communities in key processes will be crucial to tackle a set of important environmental challenges in the coming decades.

Conflict of interest

None declared.