Light-dependant biostabilisation of sediments by stromatolite assemblages

Abstract

For the first time we have investigated the natural ecosystem engineering capacity of stromatolitic microbial assemblages. Stromatolites are laminated sedimentary structures formed by microbial activity and are considered to have dominated the shallows of the Precambrian oceans. Their fossilised remains are the most ancient unambiguous record of early life on earth. Stromatolites can therefore be considered as the first recognisable ecosystems on the planet. However, while many discussions have taken place over their structure and form, we have very little information on their functional ecology and how such assemblages persisted despite strong eternal forcing from wind and waves. The capture and binding of sediment is clearly a critical feature for the formation and persistence of stromatolite assemblages. Here, we investigated the ecosystem engineering capacity of stromatolitic microbial assemblages with respect to their ability to stabilise sediment using material from one of the few remaining living stromatolite systems (Highborne Cay, Bahamas). It was shown that the most effective assemblages could produce a rapid (12-24 h) and significant increase in sediment stability that continued in a linear fashion over the period of the experimentation (228 h). Importantly, it was also found that light was required for the assemblages to produce this stabilisation effect and that removal of assemblage into darkness could lead to a partial reversal of the stabilisation. This was attributed to the breakdown of extracellular polymeric substances under anaerobic conditions. These data were supported by microelectrode profiling of oxygen and calcium. The structure of the assemblages as they formed was visualised by low-temperature scanning electron microscopy and confocal laser microscopy. These results have implications for the understanding of early stromatolite development and highlight the potential importance of the evolution of photosynthesis in the mat forming process. The evolution of photosynthesis may have provided an important advance for the niche construction activity of microbial systems and the formation and persistence of the stromatolites which came to dominate shallow coastal environments for 80% of the biotic history of the earth.

Figure 1. Erosion profiles from stromatolite material and controls measured during the winter.

A. The mean pressure required to cause sequentially increasing levels of erosion in controls. Erosion thresholds (10, 20, 50 and 75% reduction in transmission against clear water [100%], respectively) were recorded for replicate incubations with increasing incubation time (o = 12 h, ♦ = 36 h, ▪ = 60 h and Δ = 84 h). B. Comparison of the mean pressure required to cause a specific level of erosion in control systems (o = 10%, ♦ = 20%, ▪ = 50% and Δ = 75%) with time. C–D. Comparison of the mean pressure required to cause a specific level of erosion for winter series (particle resuspension causing a reduction in transmission, o = 10%, ♦ = 20%, ▪ = 50% and Δ = 75%) against period of incubation for each of the experimental sites. C. Site 1. D. Site 5 and E. Site 10. (n = 7 for all treatments).

Figure 2. Erosion profiles from stromatolite material and controls measured during the summer.

The mean pressure required to cause a specific level of erosion (particle resuspension causing a reduction in transmission, o = 10%, ♦ = 20%, ▪ = 50% and Δ = 75%, n = 7) against period of incubation for each of the experimental sites. A. Control of beach sand. B. Experimental replicates held in continuous darkness from site 1. For the penultimate incubation period, 3 replicates were transferred to the alternate condition (ambient light) as indicated by the dotted lines. C. Experimental replicates from site 1 kept under ambient light and temperature conditions. For the penultimate incubation period, 3 replicates were transferred to the alternate conditions (darkness) as indicated by the dotted lines. D. Experimental replicates from site 10 held in continuous darkness. For the penultimate incubation period, 3 replicates were transferred to the alternate condition (ambient light) as indicated by the dotted lines. E. Experimental replicates from site 10 kept under ambient light and temperature conditions. For the penultimate incubation period, 3 replicates were transferred to the alternate conditions (darkness) as indicated by the dotted lines. (n = 7 for all treatments except where stated).

Figure 3. Oxygen and calcium concentrations within the mat systems.

Depth profiles of oxygen (▪) and calcium (•) in the upper 8 mm of the sediments from site 10. Left hand side panels depict light incubations; right hand side panels represent dark incubations. Each profile corresponds to the average of three measurements. From top to bottom, measurements were taken after 12 h, 60 h, 108 h and 156 h, respectively. Average light intensities were 1613, 1241,1976, and 1846 µE m⁻² s⁻¹, during the 12 h, 60 h, 108 h, and 156 h afternoon O₂ measurements, respectively.

Figure 4. Low-temperature scanning electron micrographs of reconstituted stromatolite material.

A. Material after the first 2 days of incubation. Surface ooids and organic material. B. Organic linkages between ooid grains. C. Further development of organic material at the surface. D. Detail of ooids showing beginning of a complex matrix of polymers and cyanobacterial (Schizothrix) filaments. E–F. The cyanobacterial matrix becomes denser eventually enveloping the ooid grains. Bar markers: A = 800 um, B = 100 um, C = 400 um, D–F = 100 um.

Figure 5. CSLM images showing the initial trapping of ooids on mat surface.

A–C. The accumulation of EPS and abundant filamentous cyanobacterial cells that begin to surround ooids to form a structured microbial community. Note the autofluorescence and scattering of aragonite (blue), cyanobacterial pigment autofluorescence (red) and heterotrophic cell clusters (green). D. Sediment ooids appear orange, while EPS stained with lectin Con-A appears green. (Scale bar given in um).

Figure 6. Linear relationship between eroding pressure and time.

Linear regression lines for the equations given in Table 1. The relationships represent the increase in stability with time for the winter series from site 10 (•), the summer series from site 1 (▴) and the summer series from site 10 (▪). For clarity, the mean values of the data groups are indicated by the symbols however, the regressions were calculated using all data points.

Figure 7. Highborne Cay in the Bahamas.

The location of Highborne Cay in the Exuma chain of Bahamian Islands. A. Aerial detail of Highborne Cay. B. The samples sites from the North-easterly beach of the island as described previously .