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Sustainable construction: Toward growing biocement with synthetic biology

Published online by Cambridge University Press:  18 August 2023

A response to the following question: Can we grow a building and why would we want to?

Yuval Dorfan Open the ORCID record for Yuval Dorfan [Opens in a new window] ,
Yael Morris ,
Benny Shohat  and
Ilana Kolodkin-Gal Open the ORCID record for Ilana Kolodkin-Gal [Opens in a new window]
Yuval Dorfan*
Affiliation:
Faculty of Electrical Engineering, Holon Institute of Technology, Holon, Israel
Yael Morris
Affiliation:
Faculty of Electrical Engineering, Holon Institute of Technology, Holon, Israel
Benny Shohat
Affiliation:
Faculty of Electrical Engineering, Holon Institute of Technology, Holon, Israel
Ilana Kolodkin-Gal*
Affiliation:
Department of Plant Pathology and Microbiology, The Hebrew University of Jerusalem, Jerusalem, Israel Reichman University, Herzlia, Israel
*
Corresponding authors: Yuval Dorfan; Ilana Kolodkin-Gal; Emails: dorfany@gmail.com; ilana.kolodkin@runi.ac.il
Corresponding authors: Yuval Dorfan; Ilana Kolodkin-Gal; Emails: dorfany@gmail.com; ilana.kolodkin@runi.ac.il
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Abstract

The built environment contributes to global carbon dioxide emissions with carbon-emitting building materials and construction processes. While achieving carbon-neutral construction is not feasible with conventional construction methods, microbial-based construction processes were suggested over three decades ago to reduce carbon dioxide emissions. With time, questions regarding scaling, predictability, and the applicability of microbial growth and biomass production emerged and still needed to be resolved to allow manufacturing. Within this opinion, we will discuss what can be achieved not to ‘grow a building’ per se but to ‘grow environmentally friendly biocement’. Elaborate pathways leading to the formation of cementitious materials by genetically manipulatable microorganisms have been described so far, providing options to enhance the suitability of these pathways for construction with synthetic biology and bioconvergence. These processes can also be combined with additional beneficial properties of cement-producing organisms, such as antimicrobial properties and carbon fixation by photosynthesis. Therefore, while we cannot yet ‘grow a building’, we can grow and design biocement for the construction industry.

Keywords

Biofilmsmicrobial biotechnologymicrobiomebiomineralizationbiocement

Information

Type
Impact Paper
Information
Research Directions: Biotechnology Design , Volume 1 , 2023 , e14
Creative Commons
Creative Common License - CCCreative Common License - BYCreative Common License - NCCreative Common License - ND
This is an Open Access article, distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives licence (http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided that no alterations are made and the original article is properly cited. The written permission of Cambridge University Press must be obtained prior to any commercial use and/or adaptation of the article.
Copyright
© The Author(s), 2023. Published by Cambridge University Press

Current challenges in construction

Bacterial biomineralization was frequently considered for bioconstruction with an emphasis on bioconcrete. The overall aim is to design self-healing construction materials, and to reduce the extensive carbon dioxide emission from the construction industry, responsible for a significant portion of carbon dioxide emissions (Myhr et al., Reference Myhr, Røyne, Brandtsegg, Bjerkseter, Throne-Holst, Borch, Wentzel, Røyne and Koller2019; Zamora-Castro et al., Reference Zamora-Castro, Salgado-Estrada, Sandoval-Herazo, Melendez-Armenta, Manzano-Huerta, Yelmi-Carrillo and Herrera-May2021).

While achieving carbon-neutral construction is not feasible with conventional construction methods, a conceptual framework to ‘grow buildings’ with bacteria was suggested over three decades ago (Dade-Robertson et al., Reference Dade-Robertson, Keren-Paz, Zhang and Kolodkin-Gal2017). Cement is primarily composed of calcium carbonate from limestones and lime. The cement manufacturing sector leads 8% of the overall greenhouse gas production (CO2), growing at uncontrollable amounts as a result of speedy industrialization and the rise of the human population (Alghamdi, Reference Alghamdi2022). Furthermore, cement production is expected to exceed 6 billion metric tons by 2050 (Sharif and Tauqir, Reference Sharif and Tauqir2021). A continuous increase in near-surface atmospheric temperature is often reported, and the additional energy stored in the climate system contributes to ocean warming. Thereof, reducing carbon dioxide emissions is one of the goals of the Agenda for Sustainable Development, highlighted in Goal 13: Climate Action (Brigitte Baptiste, Reference Brigitte Baptiste2015; Durmisevic et al., Reference Durmisevic, Beurskens, Adrosevic and Westerdijk2017; Alghamdi, Reference Alghamdi2022).

Like in anthropogenic environments, in nature, construction constantly takes place. Multicellular organisms develop from a single cell embryo into complex structured organisms, containing organelles from organic and inorganic (such as bones and teeth) building blocks. Corals produce from a single polyp into 3D complex communities held together by a mineralized scaffold, and bacteria construct architectonically complex 3D communities that frequently contain mineral and organic extracellular component (Keren-Paz and Kolodkin-Gal, Reference Keren-Paz and Kolodkin-Gal2020). Unlike human bones and teeth, designed with calcium phosphate mineral (assembled over hydroxyapatite or apatite) over a collagen template (Jeong et al., Reference Jeong, Kim, Shim, Hwang and Heo2019), scaffolds formed by soil and marine bacteria and corals are frequently composed of calcium carbonate (Dhami et al., Reference Dhami, Reddy and Mukherjee2013; Phillips et al., Reference Phillips, Gerlach, Lauchnor, Mitchell, Cunningham and Spangler2013; Dardau et al., Reference Dardau, Mustafa and Aziz2021), although accumulation of crystalline calcium phosphate was also reported (Hirschler et al., Reference Hirschler, Lucas and Hubert1990). Crystals formed over the organic templates are either vaterite [generated by cyanobacteria (Zafar et al., Reference Zafar, Campbell, Cooke, Skirtach and Volodkin2022)], aragonite [generated by corals, and microalgae/cyanobacteria (Xu et al., Reference Xu, Peng, Bai, Ta, Yang, Liu, Jang and Guo2019)] and calcite formed by Bacillus subtilis and the Bacillus phylum members (Oppenheimer-Shaanan et al., Reference Oppenheimer-Shaanan, Sibony-Nevo, Bloom-Ackermann, Suissa, Steinberg, Kartvelishvily, Brumfeld and Kolodkin-Gal2016; Keren-Paz et al., Reference Keren-Paz, Maan, Karunker, Olender, Kapishnikov, Dersch, Kartvelishvily, Wolf, Gal, Graumann and Kolodkin-Gal2022), Pseudomonas aeruginosa (Li et al., Reference Li, Chopp, Russin, Brannon, Parsek and Packman2015; Cohen-Cymberknoh et al., Reference Cohen-Cymberknoh, Kolodkin-Gal, Keren-Paz, Peretz, Brumfeld, Kapishnikov, Suissa, Shteinberg, McLeod, Maan, Patrauchan, Zamir, Kerem and Kolodkin-Gal2022), and cyanobacteria (Kranz et al., Reference Kranz, Levitan, Richter, Prášil, Berman-Frank and Rost2010). These systems offer a clear advantage to the construction as potential sources for the generation of environmentally friendly cementitious materials (Yang et al., Reference Yang, Chu, Cheng and Liu2022). The regulatory principles of bacterial systems are extensively characterized (Brown, Reference Brown1992) and the genetics of biomineralization is increasingly resolved (Keren-Paz and Kolodkin-Gal, Reference Keren-Paz and Kolodkin-Gal2020), making bacterial biotechnology especially appealing for the construction industry.

Within this opinion, we will discuss the state of the art of the field allowing to grow a functional built environment microbiome. We suggest that an achievable goal is introducing self-regenerating communities producing Cementitious materials while considering synthetic biology as a tool to improve their function. Our conclusion is that while we cannot yet ‘grow a building’, we can grow and design functional bacterial species for biocement optimization.

Molecular mechanisms promoting the production of cementitious materials by microorganisms

Bacteria are well known for producing cementitious materials. For example, Sporosarcina pasteurii, Bacillus subtilis, and B. megaterium promote calcium carbonate precipitation (Oppenheimer-Shaanan et al., Reference Oppenheimer-Shaanan, Sibony-Nevo, Bloom-Ackermann, Suissa, Steinberg, Kartvelishvily, Brumfeld and Kolodkin-Gal2016; Ma et al., Reference Ma, Pang, Luo, Lu and Lin2020). While calcium is available from the environment, bicarbonate is actively produced by CO2 hydration (CO2 + H2O ↔ HCO3 + H+), where the source of CO2 can be a byproduct of bacterial metabolism or the atmosphere (Dhami et al., Reference Dhami, Reddy and Mukherjee2013). The growth of calcium carbonate crystals occurs in layers while the biogenic (organic) environment and organic polymeric substances influence crystal shape and morphology (Weiner and Addadi, Reference Weiner and Addadi2011; Zhang et al., Reference Zhang, Xie, Liu, Chen, Ping, Fu and Su2016).

In structured microbial communities (mats, biofilms and aggregates) cells are embedded in self-produced organic polymers (Flemming and Wuertz, Reference Flemming and Wuertz2019) absorb Ca2+ and promote calcium carbonate formation by providing nucleation sites. In addition to the extracellular composition, the precipitation of calcium carbonate depends on concentrations of (i) calcium ions and (ii) carbonate ions. It is also determined by two additional factors: (iii) the pH and (iv) the availability of crystal nucleation sites. The formation of the cementous minerals of calcium carbonate requires alkaline pH to promote calcium sequestration. The most widely used microbial process of CaCO3 precipitation is arguably the one based on the hydrolysis of urea. The reaction is catalyzed by the enzyme urease. Urease exerts one conserved catalytic function that is the hydrolysis of urea. The products of the reaction and the resulting increase in pH of the reaction environment that can reach pH up to 9.2. The products of the reaction are carbonic acid and ammonia (Phillips et al., Reference Phillips, Gerlach, Lauchnor, Mitchell, Cunningham and Spangler2013).

Ureolytic biomineralization is carried out with ureolytic bacterial strains (expressing detectable amount of the enzyme Urease). In addition to the bulk phase, calcite/aragonite/varterite crystallization takes place on bacterial cell walls, which serve as crystal nucleation sites. The cell walls possess negatively charged functional groups and attract and bind Ca2+ ions, resulting in their deposition and accumulation, a process that also contributes to microbial aggregation. Consequently, carbonate crystals can grow on the external surfaces of cells. The involvement of the enzymes of carbonic anhydrase (CAs), zinc-binding enzymes, that catalyze the reversible conversion of carbon dioxide and water to bicarbonate and one proton (Tripp et al., Reference Tripp, Smith and Ferry2001). Specific CAs are involved in the carbonate biomineralization in distinct metazoan lineages, including sponges (le Roy et al., Reference le Roy, Jackson, Marie, Ramos-Silva and Marin2014), and their role in microbial mineralization of calcium carbonate was also recently reported (Lotlikar et al., Reference Lotlikar, Hnatusko, Dickenson, Choudhari, Picking and Patrauchan2013; Cohen-Cymberknoh et al., Reference Cohen-Cymberknoh, Kolodkin-Gal, Keren-Paz, Peretz, Brumfeld, Kapishnikov, Suissa, Shteinberg, McLeod, Maan, Patrauchan, Zamir, Kerem and Kolodkin-Gal2022; Keren-Paz et al., Reference Keren-Paz, Maan, Karunker, Olender, Kapishnikov, Dersch, Kartvelishvily, Wolf, Gal, Graumann and Kolodkin-Gal2022).

In addition to extracellular formation of extracellular cementous materials, intracellular mineralization of amorphous calcium carbonate (ACC) (a non-crystalline material) was described in the genetically manipulatable Gram-positive bacteria Bacillus licheniformis (Han et al., Reference Han, Gao, Zhao, Tucker, Zhao, Bi, Pan, Wu and Yan2018) and Bacillus subtilis (Keren-Paz et al., Reference Keren-Paz, Maan, Karunker, Olender, Kapishnikov, Dersch, Kartvelishvily, Wolf, Gal, Graumann and Kolodkin-Gal2022). Intracellular calcium carbonate storage was also documented in photosynthetic bacteria (Xu et al., Reference Xu, Peng, Bai, Ta, Yang, Liu, Jang and Guo2019; Benzerara et al., Reference Benzerara, Duprat, Bitard-Feildel, Caumes, Cassier-Chauvat, Chauvat, Dezi, Diop, Gaschignard, Görgen, Gugger, López-García, Millet, Skouri-Panet, Moreira, Callebaut and Dagan2022), where it was considered to contribute to carbon dioxide homeostasis. The Intracellular calcium storage is expected to affect calcium carbonate deposition and therefore should be carefully considered. For example, lysed cells may release ACC to interact with the extracellular nucleators, and affect the overall net production of calcium carbonate. While intracellular CAs are the preferred targets for utilization in sustainable construction, several additional intracellular pathways associated with calcium carbonate storage were also reported in bacteria (Benzerara et al., Reference Benzerara, Duprat, Bitard-Feildel, Caumes, Cassier-Chauvat, Chauvat, Dezi, Diop, Gaschignard, Görgen, Gugger, López-García, Millet, Skouri-Panet, Moreira, Callebaut and Dagan2022). These pathways could be manipulated to control microbial mineralization once resolved.

Alkaline pH effectively promotes calcium carbonate precipitation. Therefore, in addition to ureolysis, bacterial metabolic pathways that can increase the solution pH can promote calcium deposition. These include photosynthesis, ammonification, denitrification, sulfate reduction, and formate oxidation (Hammes and Verstraete, Reference Hammes and Verstraete2002; Ganendra et al., Reference Ganendra, De Muynck, Ho, Arvaniti, Hosseinkhani, Ramos, Rahier, Boon and Kostka2014). For most, if not all, of these pathways it remains to be determined how their synthetic/biological activation will improve the performance of the strains for biotechnological application.

The potential of microbial mineralization for bioconcrete applications has been thoroughly investigated and includes, so far, the restoration of cement mortar cubes, sand consolidation and limestone monument repair, reduction of water and chloride ion permeability in concrete, filling of pores and cracks in concrete, and enhanced strength of bricks (Dhami et al., Reference Dhami, Reddy and Mukherjee2013). Overall, the richness of microbial biomineralization pathways discussed here provides a comprehensive tool set for future applications.

Enhancing the microbial performance for biocement production

An introduction artificial circuits in microorganisms with synthetic biology, now acknowledged as a useful resource to solve environmental problems, can be used to improve microbial performance as well as to generate novel microbial capacities (Heinemann and Panke, Reference Heinemann and Panke2006; Serrano, Reference Serrano2007; Hanczyc, Reference Hanczyc2020). One example of the application of synthetic biology to enhance construction materials is the engineered SEEVIX polymer, which relies on a synthetic circuit that mimics the natural process of spider silk creation by inducing the fiber’s spontaneous self-assembly (Stern-Tal et al., Reference Stern-Tal, Ittah and Sklan2022). Similar synthetic circuits discussed below can augment the biotechnological applicability of bacteria for construction.

In addition to the developments in synthetic biology, integrating bioengineering and classical engineering tools to improve microbial performance is widely recognized as ‘bioconvergence’. This approach calls for controlling the microenvironment of microbial organisms used in various biotechnological applications instead of their genetic modification. Below we will elaborate on methods from synthetic biology and bioconvergence to improve the performance of microorganisms in the construction industry. Below we will elaborate on such potential interventions in the microbiome of the building that can enhance the performance and applicability of the utilized bacteria.

Improving microbial durability to concrete

A key issue for introducing self-regenerating properties into the assembled construction material is the long-term viability of microbial cells applied to the material. These microorganisms must resist manufacturing temperature, friction and potential sterilization processes. Currently, an effort is made to comprehend the concrete microbiome (Kiledal et al., Reference Kiledal, Keffer and Maresca2021). Among other issues, the resistance of concrete microbiome to extreme alkaline conditions is mandatory. When concrete is poured, its pH is ∼12.5, higher than most known naturally alkaline environments (Kiledal et al., Reference Kiledal, Keffer and Maresca2021). An emerging application of alkaliphiles is in the construction industry, where alkaliphiles are winning growing attention to treat concrete. Alkaliphiles have been trying to make concrete surface coatings, repair concrete cracks, and engineer self-healing concretes. Alternatively, to generate reparable concrete, the microbes that alter the concrete structure are introduced from outside after the structure has been poured.

One common strategy is appending spores to concrete. Spore-forming bacteria initiate the sporulation process after stressful conditions and particularly nutrient deprivation. Spores can remain dormant for extended periods (researchers have argued for up to millions of years) (Vreeland et al., Reference Vreeland, Rosenzweig and Powers2000) and possess a remarkable resistance to environmental damage (i.e., heat, radiation, toxic chemicals, and extreme pH values) (Riley et al., Reference Riley, Schwarz, Derman and Lopez-Garrido2021). Under favorable environmental conditions, the spore initiates a process called spore germination and outgrowth, where cells will begin to grow and reproduce (Bressuire-Isoard et al., Reference Bressuire-Isoard, Broussolle and Carlin2018). In one setting, the microbial spores were mixed with mortar – a building material composed of cement, mixed with fine sands and water. In this setting lime is also added to improve durability (Jiang et al., Reference Jiang, Jia, Wang and Li2020). The microcapsule broke under force representing concrete cracking, and the embedded bacteria self-healed the cracks with self-produced minerals within three weeks (Dhami et al., Reference Dhami, Reddy and Mukherjee2013).

The alternative strategy, offering challenges and opportunities for synthetic biology, is to utilize the adaptability of certain extremophiles to concrete microenvironments. The adaptability to alkaline environments can be considered while selecting strains and consortia of microorganisms for construction and formulation (Horikoshi, Reference Horikoshi2011). Several alkalophilic or alkali-tolerant species have already been implicated for bio concrete enhancement (Mamo and Mattiasson, Reference Mamo and Mattiasson2020a), but did not always have advantage over other spore formers. For example, B. halodurans was tested, showing surprisingly less efficiency in calcium carbonate deposition than the lab strain of Bacillus subtilis, B. subtilis 168, and its poor performance was linked to reduced exopolymeric substances (for the roles of EPS in mineralization, see below) (Guéguen Minerbe et al., Reference Martinez Hernandez, Gueguen Minerbe, Pechaud, Sedran, Guéguen Minerbe, Feugeas and Lors2020). In addition to Bacillus halodurans, the halophilic B. pseudofirmus was efficient in improving cement performance (Sharma et al., Reference Sharma, Alazhari, Heath, Paine and Cooper2017).

The genomes of alkaliphiles have also been studied in detail. Alkaline pH exerts metabolic and physical challenges to the embedded bacteria, among them a reversed proton gradient, with implications for ATP production, proteins (and thereby enzyme) inactivation, and instability of membranes and DNA (Horikoshi, Reference Horikoshi1999). In alkaline niches such as soda lakes and saline freshwater, a combination of abiotic pressures, including low CO2 and metal ions concentrations, low proton gradient, and high salinity, impose a thermodynamic burden on core biological functions. These functions include but are not limited to carbon fixation, oxidative phosphorylation, and motility. Although highly diverse, alkaliphiles share two main features: the ability to maintain pH homeostasis and perform bioenergetics processes in an environment with an inverse, or ‘reversed’, chemical gradient.

These properties are attributed to the enrichment in genes for cation/proton antiporters and cation/substrate symporters. The enrichment of such transporters reflects the need to balance both PMF (Proton Motor Force) to achieve pH homeostasis and fuel energetically expensive processes such as substrate acquisition and chemotaxis. In addition, alkaliphile genomes encode many membrane-localized proton and electron-retaining proteins, such as cytochrome oxidases, which allow for the maintenance of a PMF across the membrane that favors efficient proton-coupled ATP synthesis (Horikoshi, Reference Horikoshi1999). Many alkaliphilic cyanobacteria express genes involved in CO2-concentration mechanisms, which allow for efficient carbon fixation in environments where the levels of CO2 are low and are extremely useful for carbonate biomineralization (Horikoshi, Reference Horikoshi1999; Preiss et al., Reference Preiss, Hicks, Suzuki, Meier and Krulwich2015; Rampelotto, Reference Rampelotto2016; Mamo and Mattiasson, Reference Mamo and Mattiasson2020b). All these pathways can be in theory introduced to members of the same family (e.g., genes from the alkalophilic firmicutes B. pseudofirmus can be easily introduced to the highly competent labs stain of B. subtilis, or undomesticated stains with enhanced genetic competence) (McLoon et al., Reference McLoon, Guttenplan, Kearns, Kolter and Losick2011; Parashar et al., Reference Parashar, Konkol, Kearns and Neiditch2013) (Figure 1).

Figure 1.

Summary of opportunities in enhancing the capacities of bacteria for construction. Left panel: The design of genetic circuits that could significantly enhance the performance of bacteria in environmentally friendly concrete: circuits that control the survival of bacteria in concrete (durability in concrete), enzymes that enhance calcium carbonate production with artificial inducers (9bulk calcium carbonate production) and genes involved in the biosynthesis of EPS (mineral structuring). Right panel: Methods to introduce the circuits: in a single strain, or with a few strains specialized for each function that will function as a consortium.

Artificial activation of enzymes promoting biomineralization

B. subtilis colonies can rapidly accumulate up to 20% calcium carbonate of their dry weight (Keren-Paz et al., Reference Keren-Paz, Brumfeld, Oppenheimer-Shaanan and Kolodkin-Gal2018). In addition, we and others have identified genes directly promoting biomineralization, for example, urease, carbonic anhydrase, and calcium channels. In this case, synthetic biology can efficiently generate environmentally friendly concrete: by placing the enzymes involved in biomineralization, for example, Urease and carbon anhydrase, under inducible promoters. The inducible promoters can be activated in the construction site with an appropriate inducer. The induction of Urease/carbonic anhydrase is expected to induce calcium carbonate precipitation (with an advantage to urease generating a significant local pH shift towards alkaline pH). The induction of carbonate precipitation and high pH is expected to yield higher efficiency of biomineralization at the required site. Still, it may need to be more promising regarding the control of the shape and function of the final cementitious product (Figure 1).

Applications of microbial exopolymeric substances

Growth of calcite crystals occurs in layers. The relative growth rates in the various axes may alter crystal shape and morphology and may be influenced by the biogenic (organic) environment (Weiner and Addadi, Reference Weiner and Addadi2011) and by organic polymeric substances (Dhami et al., Reference Dhami, Reddy and Mukherjee2013). In bacterial communities exopolymeric substances (EPS) are secreted and the genes that encode them are resolved. It is known that extracellular matrix absorbs Ca2+. Furthermore, the EPS contribute to calcium carbonate formation by providing nucleation sites (Dupraz et al., Reference Dupraz, Reid, Braissant, Decho, Norman and Visscher2009; Azulay et al., Reference Azulay, Abbasi, ben Simhon Ktorza, Remennik, Reddy and Chai2018). However, the exact exopolymeric substances critical for biomineralization and crystal structure remain to be determined. In B. subtilis, the effect of each EPS component was evaluated by comparing the morphology of calcium carbonate crystals. Calcium carbonate assembly within the wrinkles, 3D structures associated with enhanced EPS production was significantly reduced in all matrix mutants, consistent with the concept of mineral growth aided by nucleation sites provided by the matrix (Oppenheimer-Shaanan et al., Reference Oppenheimer-Shaanan, Sibony-Nevo, Bloom-Ackermann, Suissa, Steinberg, Kartvelishvily, Brumfeld and Kolodkin-Gal2016; Azulay et al., Reference Azulay, Abbasi, ben Simhon Ktorza, Remennik, Reddy and Chai2018). The analysis of crystal morphology in the different matrix mutants showed that matrix macromolecules interact with the mineral phase to affect the growth of calcium carbonate crystals. The interaction between the extracellular matrix components and mineral crystals was further assessed and confirmed by Fourier transform infrared analysis of the crystals (Azulay et al., Reference Azulay, Spaeker, Ghrayeb, Wilsch-Bräuninger, Scoppola, Burghammer, Zizak, Bertinetti, Politi and Chai2022; Oppenheimer-Shaanan et al., Reference Oppenheimer-Shaanan, Sibony-Nevo, Bloom-Ackermann, Suissa, Steinberg, Kartvelishvily, Brumfeld and Kolodkin-Gal2016). Similarly, in P. aeruginosa, alginate and exopolysaccharides were shown to interact with calcium and calcium carbonate (Li et al., Reference Li, Chopp, Russin, Brannon, Parsek and Packman2015; Cohen-Cymberknoh et al., Reference Cohen-Cymberknoh, Kolodkin-Gal, Keren-Paz, Peretz, Brumfeld, Kapishnikov, Suissa, Shteinberg, McLeod, Maan, Patrauchan, Zamir, Kerem and Kolodkin-Gal2022; Jacobs et al., Reference Jacobs, O’Neal, Lopatto, Wozniak, Bjarnsholt, Parsek and Bondy-Denomy2022). These results strongly indicate that using artificial overexpression constructs for exopolysaccharides or amyloids, as well as mutant strains is likely to generate differential calcium carbonate-based materials. Furthermore, the current observations provide a proof of concept for controlling the final product of bacterial construction by generating or isolatingEPS mutants for each structural element, or alternatively inducing exopolymers at desired growth direction.

The effect of EPS-based nucleation on crystal assembly is probably a general feature of biofilm mats. Importantly, the shape of the calcium carbonate crystals varies between different species. For example, Mycobacterium smegmatis that produces fatty acids-based EPS (Ojha et al., Reference Ojha, Anand, Bhatt, Kremer, Jacobs and Hatfull2005; Esteban and García-Coca, Reference Esteban and García-Coca2018) and accumulates calcium carbonate (Keren-Paz et al., Reference Keren-Paz, Brumfeld, Oppenheimer-Shaanan and Kolodkin-Gal2018). Many soil bacteria are genetically manipulable, generate versatile EPS and provide a flexible toolbox for future engineers and architects (Figure 1).

In theory, the desired calcium carbonate element to be used in biocement or building foundations can be produced by designing the composition of the bacterial communities.

Synthetic biology and bioconvergence to enhance the sustainability of buildings’ microbiome

While microbial calcium carbonate for sustainable biocement production offers significant potential advancement for the construction industry, there are several additional applications that need to be considered. Synthetic genetic circuits implemented in robust bacterial hosts (Heinemann and Panke, Reference Heinemann and Panke2006; Serrano, Reference Serrano2007) offer a different approach where the bacteria serve as dedicated biosensors engineered to detect the integrity of buildings. Relying on the available repertoire of mechanosensors characterized in bacteria as probes for the stability of construct (Cox et al., Reference Cox, Bavi and Martinac2018; Gordon and Wang, Reference Gordon and Wang2019), engineered bacteria can be used to monitor decay processes within the foundations. Coupling the detection of the damage to the formation of cementitious materials may ensure that damage is not only reported but also prevented. The successful development of bacterial-based biosensors to detect 2,4-dinitrotoluene and 2,4,6-trinitrotoluene in buried landmines is encouraging support for this application (Belkin et al., Reference Belkin, Yagur-Kroll, Kabessa, Korouma, Septon, Anati, Zohar-Perez, Rabinovitz, Nussinovitch and Agranat2017).

The formation of calcium carbonate has been studied and requires special consideration of microbial survival in soils in the context of construction foundations (Seifan and Berenjian, Reference Seifan and Berenjian2018). For this purpose, several approaches were suggested to increase the competitiveness and survival of bacteria in the complex soil microbiome and were reviewed extensively by us and others (Hou and Kolodkin-Gal, Reference Hou and Kolodkin-Gal2020; Rebello et al., Reference Rebello, Nathan, Sindhu, Binod, Awasthi and Pandey2021).

Engineered bacteria should also be considered to enhance anti-bacterial and anti-fungal activities of the construct, and thereby preventing the decay of construction materials by biodegradation. While designing dyes with anti-mold properties was frequently examined from the chemical perspective, many of the strains suggested for bioconstruction, and especially Bacillus species, are potent producers of broad-spectrum anti-fungal agents (Maan et al., Reference Maan, Itkin, Malitsky, Friedman and Kolodkin-Gal2022). While anti-mold compounds tend to have a single bioactive compound, bacteria produce multiple compounds on the same time, which can be all activated synchronically by deleting their natural repressing proteins (For example, in B. subtilis multiple antibiotics and anti-fungal compounds are regulating by a single response regulator Abh (Strauch et al., Reference Strauch, Bobay, Cavanagh, Yao, Wilson and le Breton2007) prior to introducing them into paints/construction materials.)

Conclusions

The formation of biocement is emerging as a platform to harvest natural biological processes of producing alternative construction materials for construction in an environmentally friendly manner (free of or significantly reduced greenhouse gas emissions). Before, we and others highlighted the usefulness of microbial biomineralization in genetically manipulatable bacteria for this process. While the initial focus was on designing the bacterially produced cementitious materials (Kolodkin-Gal et al., Reference Kolodkin-Gal, Parsek and Patrauchan2023; Dhami et al., Reference Dhami, Reddy and Mukherjee2013; Alghamdi, Reference Alghamdi2022), it became clear that reducing the costs and increasing the use of bacteria for cement production is more complex: The strains should be chosen or designed to endure the harsh environment of the cement well while performing the enzymatic processes that promote biomineralization, the control in the production of exopolymers that provide additional nucleation sites for carbonate minerals should be improved. It is also desired that enzymes (e.g., Urease (Anbu et al., Reference Anbu, Kang, Shin and So2016; Keren-Paz et al., Reference Keren-Paz, Brumfeld, Oppenheimer-Shaanan and Kolodkin-Gal2018; Wu et al., Reference Wu, Li and Li2021; Nodehi et al., Reference Nodehi, Ozbakkaloglu and Gholampour2022), but also additional pathways discussed above) that promote the perception of cementitious materials could be activated when required. We here (Figure 1) suggest how this can be achieved with current technologies in synthetic biology.

We conclude that while it is still challenging to ‘grow a building’, for example, manufacturing the structure from biological products of living organisms, the time is already mature to consider rebuilding the construction materials with bacteria. The informed design discussed here of available strains for the scaffolds, foundations, and shells of each building can be a conceptual leap toward sustainable construction. It is the time to grow and design the buildings’ microbiomes with improved biocement producers.

Data availability statement

All relevant data and references were included within the submission.

Financial support

The authors declare no funding was used for this work.

Competing interests

The authors declare no conflict of interest.

References

Connection references

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Figure 0

Figure 1. Summary of opportunities in enhancing the capacities of bacteria for construction. Left panel: The design of genetic circuits that could significantly enhance the performance of bacteria in environmentally friendly concrete: circuits that control the survival of bacteria in concrete (durability in concrete), enzymes that enhance calcium carbonate production with artificial inducers (9bulk calcium carbonate production) and genes involved in the biosynthesis of EPS (mineral structuring). Right panel: Methods to introduce the circuits: in a single strain, or with a few strains specialized for each function that will function as a consortium.

Author comment: Sustainable construction: Toward growing biocement with synthetic biology - R0/PR1

Published online by Cambridge University Press:  18 August 2023
DOI: https://doi.org/10.1017/btd.2023.7.pr1 [Opens in a new window]
Ilana Kolodkin-Gal [Opens in a new window] Plant Pathology and Microbiology, Hebrew University of Jerusalem Robert H Smith Faculty of Agriculture Food and Environment, Rehovot, Israel
Revision round: 0
Role: author

Comments

Dear Editors

We are here addressing the fascinating question of "Can we grow a building and why would we want to?" introduced by the Prof. Marty Dade-Robertson. Our review titled "Biosustainable buildings: Can we grow built-environment microbiomes with functional behavior?" suggests that while we cannot yet "grow a building," we can grow and design a functional building microbiome. The built environment is contributing nearly 50% of annual global carbon dioxide emission with building materials and construction responsible for 20% of the yearly carbon dioxide emission. While initial concepts were calling to build buildings from bacteria, questions regarding scaling, predictability and the applicability of microbial growth and biomass production emerged and were not resolved yet to allow manufacturing. Within this opinion, we discuss what can be achieved not to "grow a building" per se but rather to grow the functional microbiome of the building. Our review addresses the foundations, external and internal walls, and roofs of buildings as "organs" to be enhanced by synthetic biology and Bioconvergence. Overall, we suggest to enhance the sustainability of the built environment with functional microbiomes and synthetic consortia.

Sincerely,

Dr. Ilana Kolodkin-Gal

Suggested reviewers

1. Prof. Lital Alfonta, Expertise: synthetic biology, biotechnologyBen Gurion University, alfontal@bgu.ac.il

2. Prof. Yechezkel Kashi, Expertise: Biotechnology and NanotechnologyTechnion, kashi@tx.technion.ac.il

3. Prof. Ehud Banin, Expertise: BiotechnologyBar-Ilan University, Ehud.Banin@biu.ac.il

4. Prof. Marianna Patruchan, Expertise: Microbial calcium signaling, calcium carbonate depositionOklahoma State University, m.patrauchan@okstate.edu

5. Prof. Kenneth Timmis, Expertise: Microbial Biotechnology, Sustainabilityk.timmis@icloud.com

Review: Sustainable construction: Toward growing biocement with synthetic biology - R0/PR2

Published online by Cambridge University Press:  18 August 2023
DOI: https://doi.org/10.1017/btd.2023.7.pr2 [Opens in a new window]
Meng Zhang [Opens in a new window] Northumbria University, Newcastle upon Tyne, United Kingdom of Great Britain and Northern Ireland
Date of review:  13 February 2023
Revision round: 0
Role: reviewer
Recommendation/decision: major-revision

Conflict of interest statement

Reviewer is a co-author with Ilana on one paper in 2017.

Comments

I found the concept is great, but I have a few concerns regarding current version:

1) The term ‘renewable’ has been used several times by authors to describe Bio cementitious materials. I am not sure what is the definition for ‘renewable’ that authors refer to. There is assumption but lack of evidence that biocement is renewable. On the other hand, several Life Cycle Analysis based studies have suggested that MICP is potentially a better environmental option, in terms of its carbon footprint. Is ‘environmentally friendly’ the phrase more appropriate in this instance?

2) Structure of the manuscript needs to be revised. In addition, authors listed 3 goals in the built environment that aim to achieve through synthetic biology and bioconvergence, but he argument for the 2nd and 3rd goal is very weak in current manuscript which need to be strengthened significantly.

3) ‘Engineering microbial cells’ is relevant but very different from ‘Engineering Microbiome’. Authors mixed two concepts throughout the manuscript. This needs to be looked at and try to be more precise.

4) The manuscript requires English proofreading. Many sentences do not make sense and even unreadable.

5) Citation and reference format require attention.

Review: Sustainable construction: Toward growing biocement with synthetic biology - R0/PR3

Published online by Cambridge University Press:  18 August 2023
DOI: https://doi.org/10.1017/btd.2023.7.pr3 [Opens in a new window]
Date of review:  15 March 2023
Revision round: 0
Role: reviewer
Recommendation/decision: minor-revision

Conflict of interest statement

Reviewer declares none.

Comments

The manuscript Sustainable construction: Toward growing buildings microbiomes with functional behavior, aims to enhance the sustainability of the built environment with functional microbiomes that can be further improved with synthetic biology and bioconvergence.

The following review of this paper is written from an architectural perspective and examines the impact of the paper on the design and manufacturing of the built environment.

In general, the authors looked at a subject that is important and potentially impactful from the point of sustainable construction for the built environment.

The paper's main claim is that we cannot yet "grow a building" however we can grow and design a functional building microbiome. The authors support this with overarching challenges to build buildings from bacteria such as scaling, predictability, and the applicability of microbial growth and biomass production for manufacturing. To fully address this claim, the authors should define better their understanding of the term ‘growing a building’. To what part of the building lifecycle are they referring as challenging? To what type of construction method? What is the duration of such phases? For architecture? For the living organism? What about modular parts of buildings such as bricks and blocks? It is important not to generalize the claim but to communicate better the paper statement and direction.

In lines 66-68 the sentence grammar is unclear.

Line 106-107: “While CAs and Ureases are the preferred targets for sustainable construction design”. This statement is unclear, the link to construction design needs to be discussed explicitly.

Considering each building as a "halobiont” is highly interesting. While the growth constraints on the bacteria are stipulated (lines 260-263), the main observation or suggestion to the authors is to also comment on the constraints for construction. What is the impact of using such engineered materials and methods within existing and developing technologies in the context of AEC. The application of new performing materials in AEC is highly related to the development of manufacturing techniques. How do such material applications operate within such mechanisms? What are the influences of production properties (i.e. temperature, friction, sterility)? How can we relate the biological and construction manufacturing processes?

Another suggestion for the authors to promote the impact of the paper relates to its inherent interdisciplinary audience, as targeted in this journal. A main challenge is making such knowledge accessible for built environment disciplines such as construction and architecture. While the authors address clearly topics such as biological monitoring within foundations, some inspiring topics such as genetically controlling calcium carbonate production remain conceptual or non-explicitly connected to spatial domains and therefore difficult for experts in other fields (i.e. architecture) to explore scientifically.

Since the authors refer in their conclusion to scaffolds, foundations, and shells of buildings, it could be useful throughout the paper to describe which functional microbiomes and their associated behavior could relate to these building parts, the processes of designing them, and their manufacturing mechanisms.

Recommendation: Sustainable construction: Toward growing biocement with synthetic biology - R0/PR4

Published online by Cambridge University Press:  18 August 2023
DOI: https://doi.org/10.1017/btd.2023.7.pr4 [Opens in a new window]
Martyn Dade-Robertson [Opens in a new window] School of Architecture, Planning and Landscape, Newcastle University, Newcastle upon Tyne, NE1 7RU United Kingdom of Great Britain and Northern Ireland
Date of review:  17 March 2023
Revision round: 0
Role: Editor in Chief
Recommendation/decision: major-revision

Comments

The paper is highly relevant to this question and contains some interesting and useful review work especially on biomineralisation. However, the papers structure and current writing style and content need significant work and I would point to Review 1, in particular, who has requested structural changes and enhanced copy editing before publication.

From an editorial perspective the core narrative of the paper is not very clear. The main bulk of the paper deals with different approaches in nature and, harnessed synthetically of microbial mineralization to create building materials and for soil improvement. However, the title, introduction and conclusion seem to suggest that the paper is a broad framework for the ‘building microbiome’ or the ‘holiobot;’ or holobiome and contains information on, for example “generating a building microbiome with sustainable with photosynthetic capacities and enhancing the structures antimicrobial and anti fungal properties…” However, not all these topics are covered. The microbiome has a clear definition in scientific literature which refers to the sum total of all the microorganisms in the environment (in the case of the environmental microbiome) but most of these examples plus only refer to individual microorganisms. Holobiot and holobiome are much broader concepts including all organisms but the paper focuses on bacteria. The concept of a holobioytic architecture is n interesting one but not really argued for here. The idea of generating a ‘photosynthetic microbiome is not mentioned again after the introduction. Terms like bioconvergence are not well defined a seem to drift from the standard definitions in their use..etc. There are frequent issues of this sort through the paper.

I would recommend establishing what the paper is about with a clear and narrow definition that meats the content. I cans out as a potential systematic review of biomineralization for construction for example p identifying key challenges and technology opportunities. Or of it is attempting to provide a broader concept to bring in a broader range of references ad develop a clear taxonomy of methods adorn approaches for example.

In a restructured format the authors should also review the logic and consistency of the language - avoiding broad and unsubstantiated claims, e.g. “ One potential application of synthetic microbiology is to help humankind achieve and fulfill its needs.”

It would also be worth checking the veracity of the citations throughout and being carful where claims are made. I did a spot check on the claims of the built environment contributing 50% annual greenhouse emissions and 20% from construction. The Zamo-Castro reference contains no reference to these statistics. The Durmisevic reference suggests that 40% (not 50%) of Co2 emissions are from the building industry and is specific to statistics for Europe. Neither of these are authoritative sources (my understanding is that global C02 from building materials manufacture is closer to 11%) and neither backs up the claim made in the paper. Sources throughout the paper should be reviewed to asses whether they are authoritative and have been cited properly.

This paper is on the borderline but I would very much like another draft. If the authors chose to resubmit I will recommend for further review.

Author comment: Sustainable construction: Toward growing biocement with synthetic biology - R1/PR5

Published online by Cambridge University Press:  18 August 2023
DOI: https://doi.org/10.1017/btd.2023.7.pr5 [Opens in a new window]
Ilana Kolodkin-Gal [Opens in a new window] Plant Pathology and Microbiology, Hebrew University of Jerusalem Robert H Smith Faculty of Agriculture Food and Environment, Rehovot, Israel
Revision round: 1
Role: author

Comments

Dear Editors, we have revised our manuscript as indicated below: a systematic review of biomineralization, with challenges and opportunities from Synthetic biology perspective. We feel that, as biologists, this is our field of expertise and where we can offer the most accurate view. The manuscript was corrected accordingly. We thank the editor and reviewers for their critical readership and believe that our revised manuscript meets the publication criteria of Cambridge University Press.

Review: Sustainable construction: Toward growing biocement with synthetic biology - R1/PR6

Published online by Cambridge University Press:  18 August 2023
DOI: https://doi.org/10.1017/btd.2023.7.pr6 [Opens in a new window]
Date of review:  19 June 2023
Revision round: 1
Role: reviewer
Recommendation/decision: accept

Comments

No accompanying comment.

Decision: Sustainable construction: Toward growing biocement with synthetic biology - R1/PR7

Published online by Cambridge University Press:  18 August 2023
DOI: https://doi.org/10.1017/btd.2023.7.pr7 [Opens in a new window]
Martyn Dade-Robertson [Opens in a new window] School of Architecture, Planning and Landscape, Newcastle University, Newcastle upon Tyne, United Kingdom of Great Britain and Northern Ireland
Revision round: 1
Role: Editor in Chief
Recommendation/decision: accept

Comments

This draft is much improved from the previous versions and generally the writing and definitions are clearer- the review appears to be systematic and will be of value to the BTD audience. I welcome the focusing and clarification of the scientific angle of the paper. I still, however, feel that the title and the final section of the paper are ‘overstretched’.

The paper does not address the microbiome which is “the collection of all microbes, such as bacteria, fungi, viruses, and their genes in an environment” directly. Most of technologies descried are single microbes doing a specific job so I would alter the title to reflect this. Similarly the title: Sustainable construction is generic. I would choose a more explanatory and precise title: e.g. A review of microbial biomineralization technology for building construction…or bio cements… or similar. References to designing a ‘functional microbiome’ should also be removed elsewhere.

Related to 1. Focusing in on the core science and applications of biomineralization has really helped the paper and is of high relevance to our readership. However, from page 9, the, very brief, discussion of anti-bacteria and anti mould applications seems like stretching the paper too far and does not lead to a proper discussion or comprehensive review . The relevance of microfluidics is also unclear. The conclusion further introduced a new concept (holobiont) and described engineered microbiomes. This is not introduced as a concept in the main text. These concepts may be interesting in their own right but the conclusion should summarise and synthesise the research developed in the paper rather than introducing new ideas. I would like to see an enhanced conclusion which does this job. The holobiont idea might be developed for a future paper. I would revise or remove Section 4.

Related to 1 and 2, the paper should better introduce the content. It currently cause the paper an “Opinion”. It is submitted as an “Impact” paper. I think this is, more properly, a “Review” paper and should be labelled as such. A introduction that sets up the paper: “In this paper we will review the state of the art…”. Give a clear sense of the structure and make sure that the headings follow the structure.