Spatio-temporal assembly of functional mineral scaffolds within microbial biofilms

Oppenheimer-Shaanan, Yaara; Sibony-Nevo, Odelia; Bloom-Ackermann, Zohar; Suissa, Ronit; Steinberg, Nitai; Kartvelishvily, Elena; Brumfeld, Vlad; Kolodkin‐Gal, Ilana

doi:10.1038/npjbiofilms.2015.31

Cited by 92 publications

(119 citation statements)

References 65 publications

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“…Organic extracellular matrix production has been extensively studied as a means of cell-cell and cell-substrate adhesion (Branda et al, 2001(Branda et al, , 2005Kolter and Greenberg, 2006). Recently, we and others determined that precipitation of calcium carbonate contributes to the assembly of complex biofilm architecture (Li et al, 2016a,b,c;Oppenheimer-Shaanan et al, 2016).…”

Section: Bacteria-associated Precipitation Of Calcium Carbonatementioning

confidence: 99%

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Architects of nature: growing buildings with bacterial biofilms

Dade‐Robertson

Keren-Paz

Zhang

et al. 2017

Microbial Biotechnology

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SummaryIn his text ‘On Architecture’, Vitruvius suggested that architecture is an imitation of nature. Here we discuss what happens when we begin using nature in architecture. We describe recent developments in the study of biofilm structure, and propose combining modern architecture and synthetic microbiology to develop sustainable construction approaches. Recently, Kolodkin‐Gal laboratory and others revealed a role for precipitation of calcium carbonate in the maturation and assembly of bacterial communities with complex structures. Importantly, they demonstrated that different secreted organic materials shape the calcium carbonate crystals formed by the bacterial cells. This provides a proof‐of‐concept for a potential use of bacteria in designing rigid construction materials and altering crystal morphology and function. In this study, we discuss how these recent discoveries may change the current strategies of architecture and construction. We believe that biofilm communities enhanced by synthetic circuits may be used to construct buildings and to sequester carbon dioxide in the process.

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Section: Bacteria-associated Precipitation Of Calcium Carbonatementioning

confidence: 99%

“…The bacterial extracellular matrix (brown) promotes the crystals' growth in specific directions. This figure was modified fromFigure S14in(Oppenheimer-Shaanan et al, 2016).ª 2017 The Authors. Microbial Biotechnology published by John Wiley & Sons Ltd and Society for Applied Microbiology, Microbial Biotechnology, 10, 1157-1163…”

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confidence: 99%

Architects of nature: growing buildings with bacterial biofilms

Dade‐Robertson

Keren-Paz

Zhang

et al. 2017

Microbial Biotechnology

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“…The master regulator controlling the switch to a biofilm lifestyle is the repressor SinR (Kearns et al ., ). In standard laboratory settings, several cues have been associated with biofilm maturation and assembly, including oxygen deprivation (Jayaraman and Wood, ; McLoon et al ., ; Kolodkin‐Gal et al ., ; Liu et al ., ; Bloom‐Ackermann et al ., ), small molecule sensing (López et al ., ), calcium (Oppenheimer‐Shaanan et al ., ; Mhatre et al ., ) and physical cues (Asally et al ., ; Rubinstein et al ., ; Cairns et al ., ). Focusing on B. subtilis allows us to demonstrate our perspective in the context of specific mechanisms.…”

Section: Introductionmentioning

confidence: 97%

Applying the handicap principle to biofilms: condition‐dependent signalling inBacillus subtilismicrobial communities

Harris

Kolodkin‐Gal

2019

Environmental Microbiology

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Summary Bacteria in nature often reside in differentiated communities termed biofilms. These communities, which are composed of a number of functionally‐distinct cell types, are an interesting example of division of labour in microbes, and as such have been used as a system to study the evolution of cooperation. The structured population of the biofilm also plays a critical role in the persistence of infections, and biofouling of medical and industrial devices. Biofilm formation involves several stages of differentiation, which are mediated by extracellular factors secreted by cells composing the biofilm. The developmental model of biofilm formation describes this process mechanistically: specific subpopulations of cells synthesize signals within the biofilm, and promote the differentiation of other subpopulations. The handicap principle suggests that signals function because they provide reliable information regarding the state of the signaller; here, we apply the handicap principle to signalling among cells composing Bacillus subtilis biofilms, emphasizing the perspective of secreted factors as sources of information rather than solely as mediators of development. Such information could facilitate competition among phenotypically‐similar cells composing the biofilm, affecting local organizational patterns within defined subpopulations.

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“…Secondly, to our knowledge, there is so far no criterion allowing to distinguish BIM occurring in vivo from mineralization induced on decaying biological remnants, which are abundant in marine sediments, and from abiotic organic polymers (e.g., Gower and Tirrell, 1998;Oppenheimer-Shaanan et al, 2016). Calcification in cyanobacteria is not necessarily an in vivo process and may continue after the death of the colony, straddling the boundary with post-mortem cementation and early diagenesis (Bosak and Newman, 2003).…”

Section: Inability To Distinguish Between Bim and Abiotically Producementioning

confidence: 99%

Distinguishing Biologically Controlled Calcareous Biomineralization in Fossil Organisms Using Electron Backscatter Diffraction (EBSD)

et al. 2018

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Although carbonate-precipitating cyanobacteria are ubiquitous in aquatic ecosystems today, the criteria used to identify them in the geological record are subjective and rarely testable. Differences in the mode of biomineralization between cyanobacteria and eukaryotes, i.e., biologically induced calcification (BIM) vs. biologically controlled calcification (BCM), result in different crystallographic structures which might be used as a criterion to test cyanobacterial affinities. Cyanobacteria are often used as a "wastebasket taxon," to which various microfossils are assigned. The lack of a testable criterion for the identification of cyanobacteria may bias their fossil record severely. We employed electron backscatter diffraction (EBSD) to investigate the structure of calcareous skeletons in two microproblematica widespread in Palaeozoic marine ecosystems: Rothpletzella, hypothesized to be a cyanobacterium, and an incertae sedis microorganism Allonema. We used a calcareous trilobite shell as a BCM reference. The mineralized structure of Allonema has a simple single-layered structure of acicular crystals perpendicular to the surface of the organism. The c-axes of these crystals are parallel to the elongation and thereby normal to the surface of the organism. EBSD pole figures and misorientation axes distribution reveal a fiber texture around the c-axis with a small degree of variation (up to 30 • ), indicating a highly ordered structure. A comparable pattern was found in the trilobite shell. This structure allows excluding biologically induced mineralization as the mechanism of shell formation in Allonema. In Rothpletzella, the c-axes of the microcrystalline sheath show a broader clustering compared to Allonema, but still reveal crystals tending to be perpendicular to the surface of the organism. The misorientation axes of adjacent crystals show an approximately random distribution. Rothpletzella also shares morphological similarities with extant cyanobacteria. We propose that the occurrence of a strong misorientation relationship between adjacent crystals with misorientation axes clustering around the c-axis can be used as a proxy for the degree of control exerted by an organism on its mineralized structures. Therefore, precisely constrained distributions of misorientations (misorientation angle and misorientation axis) may be used to identify BCM in otherwise problematic fossils and can be used to ground-truth the cyanobacterial affinities commonly proposed for problematic extinct organisms.

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Spatio-temporal assembly of functional mineral scaffolds within microbial biofilms

Cited by 92 publications

References 65 publications

Architects of nature: growing buildings with bacterial biofilms

Architects of nature: growing buildings with bacterial biofilms

Applying the handicap principle to biofilms: condition‐dependent signalling inBacillus subtilismicrobial communities

Distinguishing Biologically Controlled Calcareous Biomineralization in Fossil Organisms Using Electron Backscatter Diffraction (EBSD)

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