Microbial Communities Of Stromatolites

BURNS P. BRENDAN, MALCOLM R. WALTER AND BRETT A. NEILAN*

Australian Centre for Astrobiology, School of Biotechnology and Biomolecular Sciences and the University of New South Wales, 2052 Australia

1. Introduction

One of the major challenges in science is to identify modern living systems that present unique opportunities to address fundamental questions in fields ranging from microbial ecology, evolution, chemical biology, functional genomics, and biotechnology. Stromatolites represent such a system. One of the earliest pieces of evidence of planetary life is in fact contained in the microfossils of stromatolites. These extant analogues provide an insight into the nature of ancient microbial systems that dominated early life on Earth (McNamara and Awramik, 1992), and may also provide clues as to their resilience over such immense periods of geological time. This review will focus on microfossil evidence from ancient stromatolites, the significant microbial diversity shown in these living systems, and recent results on lipid profiling that link stable chemical signatures with the biotic components in modern stromatolites. We will also discuss throughout how these early life analogues fit into the emerging and exciting field of astrobiology, a multi-disciplinary field of science that allows us to address fundamental questions on our own origins and existence.

2. Microfossils in Stromatolites

As might be expected, fossil microbial mats, when they are preserved as stromatolites, are known throughout the geological record from the time of the oldest well-preserved sedimentary rocks, which are 3.4-3.5 billion years old (references in Walter et al., 1976; Allwood et al., 2006; Lowe and Tice, 2007; Van Kranendonk, 2006). In the broadest perspective, from 3.5 Ga to about 0.6 Ga stromatolites are by far the most abundant macrofossils of life on Earth. What happened then or

* Professor Brett Neilan, School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney 2052, Australia. Telephone: 61-2-9385-3235. Facsimile: 61-2-9385-1591. E-mail: b. [email protected] edu.au somewhat before to lead to a great decline in abundance and diversity is controversial: the chemistry of seawater changed, microbial mats were out-competed by macroscopic algae, or that mats were grazed and burrowed by newly emergent metazoa are the main hypotheses. All are likely to be correct. From 0.6 Ga until now the pattern is uniform: stromatolites are abundant in "extreme" environments such as places that are hypersaline, hot or otherwise exotic. What such environments have in common is a paucity of grazing and burrowing metazoans, lending credence to the hypothesis that the dominant control on the distribution of benthic microbial mats is ecological pressure from metazoans. As detailed later in this review, this is further supported through microbial population analyses on living mats and stromatolites that reveal a scarcity of eukaryotes. Intriguingly, there are resurgences of stromatolites at times of extensive metazoan extinction, such as at the Permo-Triassic boundary, at about 253 Ga.

The dominance of stromatolites in the early rock record indicates that these microbial communities are a highly persistent mode of life and a significant stage in Earth's evolution. Indeed the oxygenation of the Earth's atmosphere is attributed to the oxygenic photosynthesis and other gas production performed by Archean stromatolite communities (Hoehler et al., 2001). This major step in the evolution of the geosphere contributed to the further evolution of the biosphere, such as the diversification of eukaryotic organisms observed in the Cambrian explosion. It has even been suggested that some eukaryotes may have originated from a fusion of symbiotic partners in microbial mat and stromatolite ecosystems (Nisbet and Fowler, 1999).

The oldest record of stromatolites is controversial (Brasier et al., 2002; Schopf et al., 2002). That is because it can be difficult to demonstrate the biogenicity of what are partly sedimentary structures. The original microbial mats are rarely preserved in any stromatolites, so interpretation usually relies on other features. The stromatolites of the 3.43 Ga Strelley Pool Chert of the Pilbara region of Western Australia are a good example (Fig. 1). No fossil microbes are known from those stromatolites. However, detailed mapping reveals that the form of the stromatolites varies systematically with the past environments in which they formed. A microbial ecosystem can be reconstructed in which benthic microbial mats extended from a rocky shoreline across a subtidal platform in to relatively deep water (Allwood et al., 2006). While no microfossils are known from these rocks there is degraded organic matter, kerogen, which has a carbon isotopic composition consistent with biogenicity. In other rocks of the same age and older, closely associated microfossils are abundant (Schopf et al., 2007), however their affinities are obscure.

It is not until the late Archean, at 2.5-2.8 Ga, that stromatolites became abundant, and their biogenicity is widely accepted. The most thoroughly studied examples are in the Fortescue Group in Western Australia (Walter, 1983; Figs. 2 and 3). Microfossils in a strict sense are still unknown from these stromatolites but there are abundant faint remnants of filamentous structures. In addition, there is a rich biological record preserved as carbon and sulfur isotope patterns and hydrocarbon "biomarkers", even in the absence of preserved microfossils. These have been used to indicate the presence of various microbial metabolisms in ancient samples (Kakegawa and Nanri, 2006). Further, minerals within fossil

Figure 1. 3.43 billion year old stromatolites in the "North Pole" area of Western Australia, seen in a natural vertical section. Width of the field of view about 1 m.
Figure 2. Fortescue stromatolites in outcrop near Redmont, Western Australia. (Photograph by S. A. Sweetapple.)

stromatolites can provide valuable information regarding ancient seawater chemistries, climates and other environmental parameters that influenced their deposition (Grotzinger and Knoll, 1999; van Kranendonk, 2006).

Figure 3. Thin section of Fortescue stromatolite preserved in calcite, from near Redmont, Western Australia. This is from the side of a large bulbous stromatolite; top is up. Biological filament traces are prominent. Dark laminae have prostrate filament traces (not visible here). Width of field of view is 5 mm.

Figure 3. Thin section of Fortescue stromatolite preserved in calcite, from near Redmont, Western Australia. This is from the side of a large bulbous stromatolite; top is up. Biological filament traces are prominent. Dark laminae have prostrate filament traces (not visible here). Width of field of view is 5 mm.

By the early Proterozoic, 2.5 billion years, microbial mats dominated the benthic aqueous ecosystems of the Earth. They constructed reefs as extensive as any coral/algal reefs currently extant (Grotzinger, 1989). It is still difficult to elucidate the biological affinities of the constructing microbes, but most likely the dominant organisms were cyanobacteria. However, as outlined in the following sections on the microbial diversity and lipid biomarker analyses of modern stromatolites, it is now evident that these formations are home to an incredibly diverse microbial community.

3. Microbial Diversity of Living Stromatolites

In contrast to the abundance of fossilised stromatolites, extant stromatolites are rare. The best-studied modern stromatolites are those forming in open marine waters in Exuma Sound, Bahamas (Macintyre et al., 2000), as well as those from a hypersaline marine environment, that of Shark Bay on the western coast of Australia (Logan, 1961). Extant stromatolites have also been discovered in several locations, including in a Tongan caldera (Kazmierczak and Kempe, 2006), in Green Lake, New York (Eggleston and Dean, 1976) and in Lake Clifton, Australia (Moore, 1987). We will concentrate our detailed review, however, primarily on the microbiology of the living analogues in the Bahamas and, in particular, Shark Bay.

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