Using Molecular Tools for Microbial Carbonates: History
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Tanja Bosak
,
Elise Cutts
,
,
Jian Gong

Molecular methods have successfully characterized the overall community composition of mats, pinpointed microbes involved in key metabolisms, and revealed patterns in the distributions of microbial groups and functional genes. Two promising future directions include “zooming in” to assess the roles of specific organisms, microbial groups, and surfaces in carbonate biomineralization and “zooming out” to consider broader spans of space and time. A middle ground between the two can include model systems that contain representatives of important microbial groups, processes, and metabolisms in mats and simplify visualization and hypothesis testing. These directions will benefit from expanding reference datasets of marine microbes and enzymes and enrichments of representative microbes from mats. Such applications of molecular tools should increase the utility of ancient and modern microbialites as long-term recorders of microbial processes and environmental chemistry and improve modern applications of microbial mineralization.

  • microbialites
  • microbial carbonates
  • photosynthesis
  • exopolymeric substances
  • biomineralization

1. Introduction

Fossilized microbial mats are the earliest record of life on Earth [1][2][3]. Even though the identities of individual organisms in fossilized mats remain unknown, the macroscopic sizes of lithified microbial mats—microbialites—tell that a myriad organisms must have come together to bind sediments, drape rock surfaces, form cohesive layers, and promote mineral precipitation. Most microbialites were preserved by carbonate minerals, but exceptional preservation of textures, organic matter, and microbial fossils in some Archean and many Proterozoic laminated microbialites and stromatolites also required more localized precipitation of silica. Studies of modern microbial mats and their fossilized counterparts in the 20th and the 21st century revealed the dependence of macroscopic microbialite morphologies, as well as the microscopic textures and microbial fossils in carbonate microbialites on environmental physics and chemistry; the distribution and nature of different primary producers, such as coccoidal vs. filamentous cyanobacteria; the types of microbial surfaces present; and the small-scale gradients in microbial activity (see References [4][5][6][7][8][9][10][11][12][13][14][15][16][17][18][19][20][21][22][23][24]).
Most of the microbial constituents in marine carbonate-precipitating mats are not readily identifiable by eye [7][25][26], but Cyanobacteria, the primary producers in modern microbialites, excrete copious extracellular polymeric substances (EPS) that bind sediments[7][24]. Sediment-trapping alone cannot build stromatolites—carbonate minerals precipitated in situ cement the microbialites and create some of their textures, and processes within mats could potentially influence the growth or dissolution of trapped grains, as well. Microchemical measurements and visualization techniques combined with isotope labeling and microscopy have linked the activity of sulfate reducing bacteria and cyanobacteria to carbonate precipitation and cementation in modern microbialites and carbonate grains (see References [7][8][27][28][29][30][31][32][33][34][35][36][37][38]). However, these approaches alone cannot explain the mind-boggling diversity of microbes in modern mats [39][40][41][42][43][44], confirm specific microbial interactions that effect mineralization, or predict which textures and microbialite morphologies will form.

2. Microbial Influences on Mineral Precipitation in Microbialites

Molecular techniques are one powerful means of observing and characterizing the biological factors at play in mineralization. These biological factors fall broadly into two categories: metabolic activities that change the chemical environment to promote or inhibit mineralization; and organic compounds that influence mineral nucleation, growth, ordering and shape. The precipitation and dissolution of carbonate minerals depend on the degree to which carbonate minerals are oversaturated or undersaturated in solution, which itself depends on carbonate alkalinity [4][30][45]. Microbial communities locally influence the alkalinity and the saturation state of carbonate minerals via metabolic activities that act as direct sources or sinks for carbonate ions or induce changes in the pH. An understanding of community structure and the effects of various metabolic guilds enables predictions of the net effect of this alkalinity engine.
Phototrophic CO2 fixation favors the net precipitation of carbonate minerals. Oxygenic photosynthesis takes in HCO3- and releases OH− ions to increase carbonate alkalinity and pH. Anoxygenic photosynthetic oxidation of HS− decreases alkalinity; however, simultaneous increases in pH maintain favorable conditions for precipitation. These processes are restricted to the upper illuminated parts of the mat and are offset by aerobic respiration, which favors carbonate dissolution by increasing pCO2. The effects of oxygenic photosynthesis and aerobic respiration are balanced in time. At night, oxygenic and anoxygenic phototrophs can ferment, fix N2, and contribute to denitrification— all processes that produce protons and favor dissolution. For these reasons, carbonate minerals in modern microbialites precipitate more extensively in the zones of microbial sulfate reduction and extensive organic degradation [8][31][46] and typically do not preserve the finely laminated photosynthetic textures. The activity of sulfate-reducing bacteria (SRB) is less constrained in time and space. The diversity of organic substrates, the completeness of substrate oxidation, environmental buffering, and the extent of sulfate reduction determine the degree to which sulfate reduction increases alkalinity [47][48]. Some sulfide produced by SRB can feed back into anoxygenic photosynthesis and light-independent sulfide oxidation, with the latter process particularly favoring carbonate dissolution (see References [44][49][50]). Other processes, such as iron reduction or the release of ammonia due to protein degradation, increase alkalinity and may contribute to mineral precipitation (see References [51][52]). Deeper in the mat, methanogenesis and fermentation favor carbonate precipitation and dissolution, respectively (see References [36][53][54]).
The initial nucleation of carbonate mineral phases often imposes the largest kinetic barrier to the precipitation of these minerals from oversaturated solutions. Organic molecules appear to drastically reduce this barrier and control the mineral phase and ordering (see References [55][56][57][58][59][60][61][62]). Incipient carbonate precipitates in modern microbial systems occur as nanometer-sized grains within the EPS and on cell surfaces [21][22][23][31][63][64]. Different cell or viral surfaces and microbial EPS can influence mineral grain sizes, shapes, and crystal ordering [59][65][66][67][68][69]. Thus, organic surfaces within microbial mats are just as critical to mineral nucleation, maturation, and diagenesis in microbial mats, as are major metabolisms, such as photosynthesis and sulfate reducers. These surfaces include both cells themselves, which can have different membrane or cell-wall characteristics (e.g., Gram-negative vs. Gram-positive) relevant to mineralization [70], and their extracellular secretions.
Microorganisms that live in benthic environments, and especially cyanobacteria, secrete copious amounts of EPS. The negatively charged functional groups on organic surfaces (e.g., carboxyl, acetyl, hydroxyl, succinyl, and others) can bind Ca2+ and Mg2+ and are thought to be the most important mineral nucleation sites [56][69]. These functional groups—in particular, carboxylic acids, phosphates, and amines—are typically assumed to be present in EPS by the models used to characterize EPS using titration data [71]. Such models are yet to incorporate the reports of abundant sulfate groups produced by sulfate-reducing bacteria [72], pustule-forming cyanobacteria [73][74][75], and other cyanobacteria [76]. Sulfate-rich EPS produced by pustule-forming cyanobacteria binds magnesium to promote microbial silicification in solutions that contain more silica compared to modern-day seawater [74][75]. In fact, the spatial proximity of fossiliferous cation-rich chert and texture-preserving dolomite has generated testable hypotheses about the contribution of Mg-binding microbial surfaces in the formation of both chert and Mg-rich carbonates.
EPS degradation changes the chemical structure of the extracellular matrix. This process modifies and removes functional groups [73], changes the acidity of the surfaces, renders smaller fragments of macromolecules, and releases multivalent cations back into the environment, where they can form minerals [19][20][28][29][34][69][72][77]. The downstream degradation of smaller insoluble and soluble products of EPS degradation may further promote this precipitation by fueling sulfate reduction and the alkalinity engine [33]. Accordingly, extensive carbonate mineral precipitation in modern microbialites occurs primarily in the zones of organic degradation, in voids, and outside of the active photosynthetic layer. Therefore, characterizing, tracking, and quantifying the cycling of EPS in different regions of microbial mats is critical for understanding of biomineralization in microbial systems.

3. Using Molecular Tools to Link Microbes to Mineralization in Microbialites from Shark Bay, Australia; and Highbourne Cay, Bahamas

The stromatolites and mats from hypersaline Shark Bay, Australia, and marine stromatolites and thrombolites in The Bahamas are among the world’s most prominent and well-studied microbialites [41][42]. While a comprehensive summary of past sequencing-based studies of the many extant microbial carbonate systems is beyond, these two microbialite systems are excellent case studies of how molecular techniques—principally SSU 16/18S rRNA amplicon sequencing, metagenomics, and transcriptomics—have been applied to investigate mechanisms that result in different mat morphologies and textures and influence carbonate alkalinity in marine microbial mats. To date, these studies have described the compositions of microbial communities in mats of different morphological types, at different geographical locations, and within different mat layers, and characterized the diversity of Cyanobacteria and sulfate reducers—the two functional clades with the most explicitly established links to the alkalinity engine and carbonate precipitation. More recent studies have expanded on this by measuring the expression of genes associated with photosynthesis, sulfate reduction, and EPS production and degradation in time and space.
The Shark Bay mats have been the subject of molecular ecology studies since the early 2000s [78][79]. Within one decade of the earliest molecular studies, the microbial community compositions of Shark Bay [41][80][81][82] and Bahamian [83][84][85][86][87][88] mats and microbialites had been extensively described, using small-subunit rRNA sequencing. Broadly speaking, these studies found abundant (>10%) Cyanobacteria and Proteobacteria in the Bahamian mats regardless of mat type. In contrast, Cyanobacteria typically accounted for only ~5% of the mat community in Shark Bay, where Proteobacteria, Bacteroidetes, Planctomycetes, and Firmicutes were more abundant. The reasons behind these differences remain unclear and invite questions about the functional roles of organisms from all these groups in different microbial mats.
Even before metagenomics and transcriptomics opened their respective windows on functional potential and gene expression in mats, researchers began attempting to associate the molecular ecology of mats with functions, mat textures, and mineralization potential. Early fluorescence in situ microscopy targeting the 16S rRNA of sulfate-reducing bacteria showed that these presumed anaerobes were actually active in oxygenated mat layers and in close contact with oxygen-producing cyanobacteria [35]. The greater microbial diversity of the more lithified Bahamian mat types was tentatively attributed to a greater metabolic diversity and biogeochemical conditions that would favor mineralization [85][86]. Similarly, the differences in the abundances and types of Cyanobacteria and other community components across the major classes of Bahamian stromatolites and thrombolites were hypothesized to either drive or reflect some morphological and biogeochemical differences [83][85][86]. Low eukaryotic diversity in five thrombolitic mats was interpreted as evidence against thrombolites being simply “bioturbated stromatolites” [83].
Niche differentiation refers to the spatial distribution of microbes within mats based on amplicon-based microbial community composition. This concept is often used to understand mineralization in Shark Bay and some other environments [89][90]. In arguably the most comprehensive study addressing niche differentiation in Shark Bay, Wong, Smith, Visscher, and Burns [41] combined depth-resolved 16S rRNA amplicon sequencing with biogeochemical data including oxygen depth profiles and measurements of sulfate reduction rates in two Shark Bay mat types. The differences in lithification between the lithifying smooth mats and the non-lithifying pustular mats depended on the lower abundances of Cyanobacteria and Deltaproteobacteria the latter [41]. A study also used the co-occurrence of certain taxonomic groups to motivate ecological-functional hypotheses. Specifically, the detection of Bacteroidetes, Proteobacteria, and Cyanobacteria in the upper layers of mats was interpreted as possible evidence for the “phototrophic consortia” that drive primary production and motivated an early argument for Bacteroidetes as degraders of EPS in mats [41].
As sequencing became less expensive, metagenomic studies enabled researchers to move beyond arguments based on niche differentiation and taxonomy and attempt to connect mineralization to the functional potential of mat microbes more directly [37][40][80][91][92][93][94][95][96]. Some of these studies proposed new hypotheses that linked the mat microbial community to carbonate precipitation. Khodadad and Foster [93] attributed the primary difference in functional potential between non-lithifying and lithifying stromatolitic mats in the Bahamas to the enrichment of carbohydrate-processing genes in lithifying mats. They interpreted this finding as a potential indication of enhanced EPS degradation in lithifying mats combined with the faster consumption of a wider variety of organic and inorganic sulfur-containing substrates (e.g., sulfate, thiosulfate, etc.) [93]. Sulfate commonly modifies the EPS of pustular mats from Shark Bay, Western Australia, where a combination of culturing and metagenomic analyses identified Cyanobacteria as the main producers of sulfated polysaccharides [73]. The same study proposed a connection among the ecology, chemical properties and biogeochemical cycles in lithifying pustular mats by detecting sulfatases, enzymes required to degrade sulfated polysaccharides, in a number of metagenome-assembled genomes, quantifying sulfatase activity and associating carbonate precipitates with areas with fewer cyanobacteria and less sulfate-rich EPS.
Comparisons among the metagenomes of different mat types in Shark Bay and The Bahamas motivated qualitative hypotheses regarding the relative importance of photosynthesis and heterotrophy in driving the carbonate alkalinity engine. A combination of metagenomic and biogeochemical data from Bahamian thrombolites pointed to photosynthesis as the most important driver of mineralization in thrombolites [95]. In contrast, Ruvindy, White, Neilan, and Burns [37] argued that the greater prevalence of predicted photosynthesis genes in the metagenomes of Bahamian mats compared to Shark Bay mats could indicate that Shark Bay biomineralization is driven more by heterotrophy than by photosynthesis. Different abundances of genes from different functional pathways in the metagenomes from adjacent stromatolites and thrombolites in Highbourne Cay and Shark Bay were interpreted as evidence that some as-yet opaque aspect of microbial community metabolism could underpin their differing mineral fabrics [97]. Most recently, transcriptomics has allowed researchers to track gene expression in mats, particularly those associated with photosynthesis and heterotrophy [95][97][98][99]. Depth-resolved metatranscriptomics of Bahamian thrombolites characterized gene expression at midday and, unsurprisingly, found more gene transcripts in pathways related to photosynthesis relative to anaerobic respiration [97]. Most of the photosynthesis gene transcripts were associated with cyanobacterial genera closely related to Dichotrix sp. (order Nostocales), the dominant cyanobacterial clade in Bahamian mats [97]. A subsequent year-long transcriptomic survey identified the filamentous Rivulaceae and coccoidal Xenococcaceae as the most active members of the community in the Bahamian thrombolites [94].
The metatranscriptomic analyses of the microbial activity over seasonal and diel cycles and in multiple mat types in Shark Bay that included cyclone-derived materials (EPS-rich cobbles and sludge) found abundant and active Bacteroidetes and sulfate-reducing bacteria in the EPS-rich cobbles [98]. Heterotrophic degradation of EPS by Bacteroidetes coupled to sulfate reduction could explain the greater amount of carbonate found in cobbles relative to sludge. This may be the first time that an explicit link between carbonate alkalinity and the activity of Bacteroidetes—an abundant phylum in Shark Bay and Highbourne Cay—has been proposed. Elevated transcription of sialic acid and aTMP–rhamnose synthesis pathways in the cobbles was also interpreted as an indication that there could be two different kinds of EPS present in cobbles, each contributing to the matrix’s resilience against degradation or cohesive properties in different ways that could potentially impact the shape and preservation of cobbles [99]. The high functional potential of Bacteroidetes, Planctomycetes, Verrucomicrobia, Chloroflexi, Myxococcota, and a few other microbial groups from pustular mats in Shark Bay for the degradation of sulfated EPS supports inferences from the transcriptomic data [73]. Molecular tools can now proceed to identify organisms involved in these pathways and their connections to the activities of Cyanobacteria, sulfate-reducing bacteria, and the many other microbial groups in the mats.

This entry is adapted from the peer-reviewed paper 10.3390/geosciences12050185

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