Microbialites—sedimentary rocks with fabric that reflects the influence of benthic microbial communities1—capture biogeochemical interactions between microbes and their environment throughout Earth’s history e.g., 2,3. Microbial mats are often considered steady-state ecosystems whose constituents consume each other’s metabolic products4. To be preserved as microbialites, organic trapping and binding of sediment alone is insufficient because eventually organisms in the lower parts of the mat consume the material binding grains5. Canonically, then, propitious microbial metabolisms drive microbialite formation by promoting authigenic cementation e.g., 6,7. Lithification occurs most readily where microbial processes within the mat locally increase carbonate mineral saturation, typically in environments where photosynthesis exceeds respiration and fermentation rates8–10. However, microbial metabolisms that inhibit lithification can only do so by consuming the products of other metabolisms that promote lithification—at worst, there can be no net diminishment of favorable ambient conditions for lithification. Microbial mats often grow in environments otherwise characterized by widespread carbonate precipitation, so why do they rarely form microbialites? We find insight into this apparent paradox on Little Ambergris Cay, Turks and Caicos Islands, where the net metabolic activity of widespread microbial mats inhibits—rather than promotes—lithification.
Little Ambergris Cay formed in the lee of Big Ambergris Cay at the eastern end of a 20 km-long ooid shoal, near the eastern margin of the Caicos platform (Fig. 1a)11–14. The shoal is characterized by well sorted medium sand-sized ooids with hardgrounds, grapestone sand, and cemented intraclasts on its northern flank11,15–17. Little Ambergris Cay (Fig. 1b) grew through shoreface accretion of ooid sand18. Eolian ridges rim a shallow interior basin that contains sand flats with widespread microbial mats (Fig. 1c)11,18–22. Foreshore and interior basin sands are less well sorted and contain more skeletal allochems than the shoal, especially where concentrated in tidal lags15,16,18.
Three microbial mat types occur in the interior basin: smooth mats, tufted polygonal mats, and colloform blister mats18,19. In the shallowest subtidal parts of the interior basin, smooth mats form pigmented mucilaginous blankets covered in beige extracellular polymeric substances (Fig. 1d). On intertidal sand flats and around mangrove thickets, polygonal mats form dark green decimeter-scale domal biscuits, often with millimeter-scale dark gray-green filamentous tufts (Fig. 1e). In supratidal environments on interior flanks of the eolian ridges, blister mats form centimeter-scale fenestral dark green to gray colloform bumps (Fig. 1f). Discontinuous crusts less than 1 cm thick underlie some mats, but many mats grow on poorly cohesive ooid sand. The upper few millimeters of ooid sands are often stabilized by microbial communities that may desiccate to form the crusts or be dislodged to form flat, angular intraclasts. All three mat types contain similar microbial communities, indicating that their textures reflect environmental controls more so than taxonomy18–21. The mats contain benthic foraminifera and cerithid gastropods (Fig. 1f), and calcareous (e.g., Halimeda and Penicillus) and non-calcareous algae (e.g., Bataphora) live in subtidal portions of the interior basin.
SEDIMENTS BENEATH MICROBIAL MATS
Eight vibracores (Fig. 1b) were collected across Little Ambergris Cay in August 2017. Vibracores, up to 3 m long, included active microbial mats up to 12 cm thick (Fig. 2a) above ooid sand with lesser skeletal sand to gravel and ooid grainstone intraclasts (Fig. 2b). Skeletal material was predominately disarticulated and/or fragmented coralline red algae, calcareous green algae (mainly Halimeda), cerithid gastropods, venerid and arcoid bivalves, benthic foraminifera, and serpulid worm tubes. Ooid grainstone intraclasts included angular, flat 1 to 4 cm flakes and rounded 3 to 5 cm nodules preserving cm-scale burrows and macroalgal holdfasts. Muddy ooid or foraminiferal sand layers represented less than 5% of the sediment and were 1 to 5 cm thick. Below about 1 m, the cores were partially indurated, occasionally preserving burrows, holdfasts, and ripple cross lamination (Fig. 2c). In thin sections, ooid-skeletal sand was heavily microbored and displayed pervasive fabrics indicative of dissolution, including solution-enlarged microbores, irregular grain boundaries, and selective leaching of micrite envelopes and micritized borings (Fig. 2d). Calcium carbonate δ13C values in the sediment ranged from 3.8 to 5.2‰ and increased with depth in the uppermost 50 cm of the cores.
Apart from the active mats at core tops, organic material was mainly limited to rare plant debris. Beneath blister mats on the edge of a tidal channel (core VC-05), we found a single occurrence of faintly laminated organic material in a 2 cm-thick, tan, muddy ooid-cerithid gastropod layer at 60 cm depth (Fig. 2e). This material displayed characteristic spectral features of chlorophyll a and bacteriochlorophyll a pigments—two main light-gathering pigments seen in the polygonal mats18.
An isolated occurrence of calcified, decimeter-scale bulbous domes was found rimming a 1.4 m-deep pond in the accretionary beach ridges on the windward facing southern part of Little Ambergris Cay (Fig. 2f). The pond, surrounded by shrubland vegetation, was filled with tannic, salinity-stratified (43 to 48 ppt), hypersaline water. The domes comprised centimeter-thick fenestral palisades of carbonate-coated filaments and mangrove leaves (Fig. 2g). These mineralized bulbous domes were unlike any of the three mat textures elsewhere on the island. Decaying microbial mats were observed in summer 2016 but were not present when the crusts were resampled in 2017; nearby ponds did contain active mats.
POREWATER GEOCHEMISTRY
Porewater was sampled from 3 vibracores situated in low supratidal polygonal mats (VC-01), intertidal polygonal mats (VC-03), and a subtidal, muddy Batophora algal substrate (VC-04). Stations for groundwater sampling at low and high tide were installed across a tidal bar and channel (Fig. 1b) at 0.2, 0.5, and 1 m depths. Water was also sampled at 7 depths from the hypersaline pond at the southern end of the cay (Fig. 1b). Porewaters, groundwaters, and pond waters ranged from normal marine to hypersaline (34 to 50 ppt), and evaporation factors relative to platform seawater, calculated from chlorinity data, ranged from 1 to 2.4 (Fig. 3). The highest evaporation factors were observed in the supratidal core, VC-01. Groundwater was salinity-stratified at high tide, with ca. 40 ppt water at 1 m below the surface. At low tide, groundwater was temperature-stratified, as surface waters warmed above 33°C while water at 1 m depth only warmed to 29°C.
DIC and alkalinity ranged from seawater concentrations (ca. 2.1 mmol/kg) to 6.01 mmol/kg in the pond surface water and to 10.81 mmol/kg in porewater (Fig. 3). Chloride-normalized sulfate concentrations ranged from 17% lower to 18% higher than seawater, and sulfide concentrations were up to 1.76 mM. Porewater DIC δ13C values increased with depth from -6.1‰ to 0.5‰. Groundwater and pond DIC δ13C values also increased with depth, but uppermost water was about -2‰. Calculated aragonite saturation states (Ω) in intertidal cores were less than 2.5 but exceeded 6 in the supratidal core. In the pond, Ω generally decreased with depth from 18.8 to 2.2. Groundwater chemistry varied substantially through a tidal cycle, with transient aragonite saturation indices as low as 0.1 and as high as 17.
CONTROLS ON MAT PRESERVATION
The Caicos platform exhibits widespread inorganic precipitation as ooids and hardgrounds and has surface seawater supersaturated with respect to aragonite11,15,17. These conditions should permit cementation that would preserve microbial mat textures throughout the interior basin, but the microbial mats remain unlithified. The thin muddy layer with poorly preserved, pigmented, laminated organic material—likely a decaying, buried mat—did not capture residual textures that would be identifiable in a microbialite (Fig. 2e). Cored sediments were compositionally similar to the ooid-skeletal sand to gravel found on the open shoal and shoreface environments around Little Ambergris Cay, but the presence of minor amounts of mud in some intervals (Fig. 2e and Supporting Information) indicated that sedimentary textures developed in an episodically lower-energy environment. Angular crust intraclasts, cerithid gastropods, and minor mangrove debris—features unique to the interior basin—were found throughout the cores. This indicates that cored ooids formed in a shoreface or shoal environment and were transported to and reworked in a restricted environment by storms, tidal currents, and bioturbation. The modern interior basin environment is dominated by mats, so we infer that mats were present in the past but not preserved beyond the rare horizons of decaying organic material. We cannot resolve when mats first colonized Little Ambergris Cay, nor predict if a future sedimentary package might preserve a facies change from massive ooid-skeletal grainstone to one more diagnostic of mat colonization. Nonetheless, lithification of the extant mats is inhibited and therefore their preservation is unlikely.
Two synergistic processes limit lithification in the shallowest subsurface: efficient organic matter decay and tidal pumping of oxidants and dissolved organic matter. Aerobic respiration and oxidation of sulfide to sulfate decrease Ω by adding DIC, removing alkalinity, or both. In response to this, aragonite sand dissolves, adding DIC and alkalinity to subsurface waters until porewaters reach aragonite saturation (Fig. 4a). Tidal pumping enables net aragonite dissolution (Fig. 3d). At low tide, sulfate reduction occurs beneath a thermally stratified upper groundwater lid, and groundwater seepage of saline, sulfidic water with high Ω emerges in tidal channels. At high tide, seawater seeps into the shallow subsurface, oxidizing sulfide and driving aragonite undersaturation. In core porewaters, sulfate depletions relative to chlorinity represent net microbial sulfate reduction in excess of the observed sulfide concentrations. In iron-poor carbonate sediments, most of the sulfide produced is reoxidized24,25. Sulfate excesses of up to 18% indicate that sulfide is not always reoxidized in situ. Mangrove root xylem tissue on Little Ambergris Cay contains sulfate with 34S/32S nearly 30‰ lower than that of seawater sulfate, suggesting that the oxygenic mangrove roots facilitate sulfide oxidation in the groundwater26. Sulfidic groundwater dynamics on Little Ambergris Cay therefore differ from those in euxinic tidal ponds in fine-grained sedimentary environments, in which the delivery of oxidants are limited by diffusion and consequently the fraction of sulfide that is reoxidized is low27.
Carbon isotope measurements provide a means to identify the carbon sources in groundwater. Inorganic carbon sources in this system include seawater DIC that has a δ13C value of ~0.85‰, ooid sand that has a δ13C value of ~5‰, and atmospheric CO2 that has a δ13C value of ~-8‰15,28. Organic matter in the microbial mats has a δ13C value of ~‑13‰19,26. In the shallowest porewater, which had the lowest DIC δ13C values (Fig. 4c), carbon isotope mass balance dictates that about half of the DIC derived from remineralized organic material and the remainder from subequal parts seawater and dissolved carbonate, consistent with the stoichiometry of respiration-driven dissolution driven by complete oxidation of organic matter to CO2 (Fig. 4b). Slightly lower δ13C values of carbonate sand within the uppermost 50 cm of cored sediments (Fig. 3) additionally suggest that a low δ13C phase may precipitate in the shallowest sediments and/or preferentially dissolve at depth; this may be selective dissolution of micrite envelopes and solution enlargement of microbores (Fig. 2d and Supplemental Information)29.
Porewater compositions evolved with depth from the shallow endmember (comprised of DIC from respired organic matter and respiration-driven dissolution of aragonite) towards a mixture of seawater and a high DIC endmember (10.8 mmol/kg) that has a δ13C value of -1.25‰ (Fig. 4c). Groundwater salinities were normal marine to hypersaline (Fig. 3), indicating that atmospheric CO2 dissolved in fresh, meteoric water did not drive significant dissolution or contribute measurably to the subsurface DIC inventory. Similarly, seawater-derived DIC would have had to have been concentrated nearly three-fold by evaporation for its admixture to satisfy the groundwater δ13C composition without additional organic carbon or dissolved carbonate input, but no such high-salinity waters were observed (Fig. 3). Thus, further dissolution of carbonate sand in the subsurface below the mats contributed to the DIC with high δ13C values.
The stoichiometry of respiration-driven dissolution makes the prediction that the deep groundwater in equilibrium with aragonite should have nearly 50% of the DIC from respired carbon (Fig. 4a), but the DIC δ13C budget indicates that only approximately 30% of DIC derived from respired organic matter (Fig. 4d). To reconcile this, carbon must leak out of the subsurface. For example, incomplete oxidation of butyrate or lactate by sulfate reducing microorganisms produces acetate and sulfide (Fig. 4b). These organic acids could flush out during ebb tides but would not oxidize as readily as the sulfide during tidal inundation with oxic waters—a process that occurs rapidly even in the absence of microbial catalysis. This leak of partially oxidized, dissolved organic material out of the Little Ambergris system was observed as plumes of brown, tannic groundwater seeping from tidal channels (Supplemental Information).
MICROBIALITE TAPHONOMIC BIAS
Across the vast majority of Little Ambergris Cay, expansive mats developed throughout the island interior do not lithify despite widespread inorganic precipitation of ooid sand, crusts, and hardgrounds. Over the entirety of the island’s surface and subsurface ecosystem, microbial processes result in net dissolution that inhibits preservation of mats—and, in fact, dissolves both autochthonous and allochthonous carbonate—regardless of any microbial processes within the mats that may modulate calcium carbonate precipitation. In other words, the microbes in very shallow groundwater, especially sulfate reducing organisms, interact with the mats and ultimately limit their organic preservation or lithification.
To drive lithification, processes such as evaporation or photosynthesis must create enough carbonate mineral supersaturation that cement precipitation rates exceed the rate saturation is decreased by aerobic respiration and sulfide oxidation to sulfate7,30. Little Ambergris Cay is dominated by these processes inhibiting lithification—facilitated by tidal advection—that result from this microbial ecosystem’s high gross productivity but low net productivity. Microbial processes that might have aided carbonate precipitation (e.g., oxygenic photosynthesis and anaerobic respiration) create products (e.g., organic matter and sulfide) that enable net dissolution. This results in interior basin surface waters that have lower aragonite saturation states (4.3) than the surrounding platform waters (4.5 – 5.6), in spite of higher salinities and extensive benthic photosynthesis15. Consequently, the thick, luxuriant mats present across Little Ambergris Cay are not preserved in the subsurface. Perhaps unsurprisingly, ancient carbonate rocks rarely contain evidence for textures that look like lithified microbial peats31. From the perspective of preservation, a robust microbial ecosystem can be too much of a good thing—fueling rapid respiration and preventing early lithification.
Given a certain carbonate mineral saturation state as a boundary condition, factors that would promote microbialite preservation include higher organic carbon burial efficiency, less dioxygen delivery, or more iron (permitting sulfide removal as pyrite). The limited encrusted domes along the pond rim (Fig. 2f), interpreted as lithified mats, provide an important example. Recalcitrant plant material in the pond may decay more slowly than the microbial mats, or saline, turbid conditions in the pond may limit robust mat growth and respiration compared to the interior basin. Incomplete respiration of organic matter and diminished tidal advection permit calcification to proceed. Similarly, sediment-rich mats, such as those forming subtidal stromatolites in other Bahamian tidal channels, may also have less productivity and slower respiration, allowing ambient conditions to control lithification6,9.
Seafloor cementation and sediment trapping and binding have demonstrable roles in microbialite formation. While microbial mats are the sine qua non of microbialites, our observations suggest that mat productivity also influences preservation. Mats in sandy, high-energy depositional environments with permeable sediments and advective water fluxes that supply plentiful dioxygen may be especially prone to decay. Somewhat paradoxically, perhaps the most productive past mats are rare or absent in the rock record.