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-Science Reviews 96 (2009) 163–172

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Earth-Science Reviews

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Flat laminated communities

Jonathan Franks, John F. Stolz ⁎

Department of Biological Sciences, Duquesne University, Pittsburgh, PA 15282, United States article info abstract

Article history: Flat laminated microbial mats are complex microbial that inhabit a wide range of environments Received 28 January 2008 (e.g., caves, springs, thermal springs and pools, salt marshes, hypersaline and lagoons, Accepted 24 October 2008 and petroleum seeps, mounts, vents, dry valleys). Their structure is defined by Available online 6 November 2008 physical (e.g., quantity and quality, , density and pressure) and chemical (e.g., , oxidation/reduction potential, salinity, pH, available acceptors and donors, chemical species) Keywords: microbial mat parameters as well as species interactions. The main primary producers may be photoautotrophs (e.g., oxygenic , , phototrophs) or chemolithoautophs (e.g., colorless oxidizing anoxygenic phototroph ). Anaerobic phototrophy may predominate in organic rich environments that support high rates of microbiolite respiration. These communities are dynamic systems exhibiting both spatial and temporal heterogeneity. They are characterized by steep gradients with microenvironments on the submillimeter scale. Diel oscillations in the physical-chemical profile (e.g., oxygen, sulfide, pH) and are typical for phototroph-dominated communities. Flat laminated microbial mats are often sites of robust biogeochemical cycling. In addition to well-established modes of for phototrophy (oxygenic and non-oxygenic), respiration (both aerobic and anaerobic), and , novel energetic pathways have been discovered (e.g., nitrate reduction couple to the oxidation of , sulfur, or ). The application of culture-independent techniques (e.g., 16S rRNA clonal libraries, metagenomics), continue to expand our understanding of species composition and metabolic functions of these complex ecosystems. © 2008 Elsevier B.V. All rights reserved.

Contents

1. Introduction ...... 163 2. Physical–chemical environment ...... 164 2.1. Light quantity and quality ...... 165 2.2. Temperature ...... 166 2.3. Oxygen ...... 166 2.4. pH ...... 166 2.5. Salinity ...... 166 2.6. Electron acceptors and donors, and chemical species ...... 167 3. Community structure...... 167 4. Advances in techniques...... 168 5. Summary ...... 169 Acknowledgements ...... 169 References ...... 169

1. Introduction

Microbial mats are communities of that colonize surfaces. They range in complexity from simple, almost mono-species fi ⁎ Corresponding author. Tel.: +1 412 396 6333; fax: +1 412 396 5907. bio lms, to multi-layered ecosystems containing diverse populations of E-mail address: [email protected] (J.F. Stolz). and small (e.g., , unicellular )

0012-8252/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.earscirev.2008.10.004 164 J. Franks, J.F. Stolz / Earth-Science Reviews 96 (2009) 163–172

arranged into assemblages and guilds (Stolz, 2000). Typically associated with the / interface these communities interact with the sediment, trapping and binding particles and clastics, and in some cases inducing precipitation and lithification (Stolz, 2003, Dupraz and Visscher, 2005). These activities in concert with the predominant mineralogy (e.g., clay, silt, siliciclastic, evaporite, carbonate) can impact the structure and fabric yielding with distinctive characteristics (e.g., micro- biolites). The structures can be preserved in the rock record and their interpretation can be enhanced by the study of modern microbiolites (Grotzinger and Knoll, 1999; Des Marais, 2003; Tice and Lowe, 2004; Noffke, 2007). and are organosedimentary structures that commonly have a vertical profile that protrudes above the horizontal plane (Monte, 1976; Reid et al., 1995, 2000). Flat laminated microbial mats rarely form relief above the horizon (e.g., desiccation cracks, Fig. 1), but the layered sediments they produce may extend to some depth below the surface (e.g., a few centimeters to meters) (Figs. 1 and 2). They thrive in a wide range of including extremes in pH (e.g., acidic sulfur caves and iron springs), temperature (e.g., thermal springs and pools, deep sea vents), and salinity (e.g., salt marshes, hypersaline ponds and lagoons), as well as ones with chemolithotrophic sources of (e.g., methane seeps, sea mounts). Their ecological success is a reflection of the metabolic versatility and physiological adaptability found within the Bacteria and . Flat laminated microbial mats are models for microbial and have been studied extensively under the auspices of and as they represent the modern analogs to ancient and possibly extraterrestrial ecosystems (Des Marais, 2003). Over the past twenty odd years several volumes have been published dedicated to microbial mats (e.g., Cohen et al., 1984; Cohen and Rosenberg, 1989 Stal and Caumette, 1994, Riding and Awramik, 2000, Krumbein et al., 2003, Inskeep and McDermott, 2005a). The purpose of this review is to present a synopsis of the current concepts, highlight some of the recent discoveries, and provide a glimpse at what lies ahead with application of new technologies.

2. Physical–chemical environment

Species occurrence and in microbial mats are strongly influenced by the physical properties and the chemical parameters of a Fig. 1. Sippewissett Marsh, Massachusetts. A) Field photo facing westward, B) Close up given environment. Important physical properties include light (both showing flat laminated mat on surface. quantity and quality), temperature, and pressure. Key chemical

Fig. 2. Flat laminated mat at Laguna Figueroa, Baja California, . A) Field photo facing eastward, B) Cross section of laminated sediments. The top 3 mm is the seasonal sediment accreting community. J. Franks, J.F. Stolz / Earth-Science Reviews 96 (2009) 163–172 165 parameters include oxygen, pH, oxidation/reduction potential, salinity, and available electron acceptors and donors, as well as the presence or absence of specific chemical species. In this section, specific properties and parameters that create unique environments that support microbial mat communities are presented.

2.1. Light quantity and quality

Photoautotrophic communities depend on both the appropriate amount of light (e.g., light quantity) and the particular (e.g., light quality) that can be used by the light harvesting and . The average amount of light that illuminates a surface on a sunny day is 1000 to 2000 μE/m2/s. Depending on the environment, however, light absorption and scattering can be significant. Particles and populations of readily attenuate light in the water . Sediment type can impact the depth at which light can penetrate into the subsurface. This light scattering can be significant resulting in the scalar being greater than the downward irradiance (Des Marais, 2003). Most phototrophs are adapted to low light intensities and often are photoinhibited. The optimum light intensity for cyanobacteria in the microbial mats of Mellum Island in the North Sea is 50 to 150 μE/m2/s. from the same mats use from 5 to 10 μE/m2/s (Stal et al., 1985). Mat communities have a variety of strategies to obtain the appropriate amount of light. Cyanobacteria produce and other light attenuating products (e.g., ), or may lie beneath a coating of sediment (Palmisano et al., 1989). Conversely, some photo- trophs are extremely adept at capturing rare in light-limited environments. e containing have been found at 100 m depth in the (Manske et al., 2005). Green sulfur bacteria are particularly well suited for low light as they can produce large numbers of light harvesting structures (e.g., chlorosomes) and have a high ratio of accessory to reaction center (Jochum et al., 2008). The Black Sea chlorobia, for example, are capable of photoautotrophy with only 0.015 μmol quanta m−2 s−1 (Manske et al., 2005). Geographic location can be important with respect to the growing season of mats. While equatorial mats see little annual change, northern and southern latitudes are subject to seasonality, while artic and systems are subject to month long extremes of constant light or darkness. Phototrophic organisms have evolved light harvesting structures and photosystems that utilize different wavelengths of light. Cyanobacteria have with a (680 nm) and (e.g., , ), green phototrophs have chlorosomes with bacteriochlorophyll c (740 nm), d (725 nm), or e (714 nm), and purple phototrophs have intracytoplasmic membranes with either bacteriochlorophyll a (800–890 nm) or bacteriochlorophyll b (1015 nm) (Stolz, 2007). These different photosystems allow a variety of phototrophic microorganisms to coexist, often forming distinct guilds and assemblages. Water is a natural attenuator of light, absorbing most of the wavelengths within the first meter. Paradoxically, it is the longer wavelengths that penetrate further into shallow water sediments (Jørgensen and Des Marais, 1986; Jørgensen et al., 1987; Pierson et al., 1987; Polerecky et al., 2007). Thus anoxygenic green and purple phototrophs can predominate certain layers (Fig. 3) and make a significant contribution to the and primary of the mat (D'Amelio et al.,1987; Stolz,1990; Nuebel et al., 2001; Polerecky et al., 2007). Flat laminated mats found in very shallow pools, lagoons, and salt marshes often have a distinct layer of anoxygenic purple

Fig. 3. Community structure in the flat laminated microbial mat from Laguna Figueroa, Baja California, Mexico. A) Surface 0–1 mm showing bundles of filaments of Microcoleus chthonoplastes.B)Subsurface1–2mmshowingfilaments of M. chthonoplastes and Chloroflexus-like filamentous green bacterium. C) Subsurface 2–3 mm with Chloroflexus- like filamentous green bacterium. Samples were glutaraldehyde fixed (2.5% in seawater buffer) and observed by Confocal Scanning Laser Microscopy (Leica TCS SP2), with excitation at 488 nm and emissions at 644–722 nm and 507–536 nm. (C) Chloroflexus-like filamentous green bacterium, (M) M. chthonoplastes, (N) . All figures have the same magnification, bar 20 μm. 166 J. Franks, J.F. Stolz / Earth-Science Reviews 96 (2009) 163–172 phototrophs with bacteriochlorophyll b below layers of cyanobacteria, overlying water column, in situ oxygenic , aerobic and purple and green phototrophs (Nicholson et al., 1987; Pierson et al., respiration and sulfide production (by sulfate reducing bacteria) 1987; Stolz, 1990). principally determine the depth profile of the oxic/anoxic transition zone (OATZ) (Canfield and Des Marais, 1993). The profile usually 2.2. Temperature follows a diurnal pattern in which the greatest net oxygen production occurs in the middle of the day (Visscher et al., 1998)(Fig. 4). There Microbial mats have been found in the frozen Antarctic (Priscu et al., are cases, however, in which the peak is in late morning as the 1998; Taton et al., 2003; Jungblut et al., 2005), as well as by hot springs intensity of the noon-day can inhibit photosynthesis (Miller et (Ward et al., 1998; Roeselers et al., 2007) and thermal vents (Alain et al., al., 1998, Jonkers et al., 2003). Typically, the oxygen in 2004; Nakagawa et al., 2005). , organisms adapted to the surface of the mat is at equilibrium with the overlying water extreme cold, are often oligotrophic, living on trace , and column but increases with depth in the first few millimeters, then having long generation times. Hot springs provide a temperature range rapidly decreases. At , a combination of respiration and from boiling at the source (100 °C at sea level, slightly lower, ~92 °C, at sulfidogenesis combine to move the OATZ closer to the surface. This higher elevations) to ~40 °C down stream with different microbial diel shift is often accompanied by the movement of motile microbial populations existing along the gradient. The temperature of water species (e.g., sp.) in response to the change (Hinck et al., flowing from a deep sea thermal vent may exceed 400 °C as it is under 2007). The activity of the oxygenic phototrophs (e.g., cyanobacteria) extreme pressure (Zierenberg et al., 2000). Nevertheless, physiologically can also affect the oxidation reduction potential (Eh) of the sediment, diverse Archaea and Bacteria exist at elevated and resulting in Eh values as high as 400 mV in the oxic zone (Visscher extensive microbial mats can develop, supported by chemolithoauto- and Stolz, 2005). trophy. The organisms associated with thermal springs and vents are distributed based on their temperature optimum, and of the 2.4. pH same species may exist at different temperatures (Ward et al., 2006; Bhaya et al., 2007). While photosynthesis seems to be limited to The pH of the environment can have an impact on microbial temperatures below 75 °C (Madigan, 2003), sulfur, iron, and nitrogen community composition as it affects an 's wall integrity, metabolism can occur at higher temperatures (Stetter, 1999, Ferrera and and the ability to produce energy as well as obtain certain nutrients. Reysenbach, 2007). The current record for nitrogen fixation is 92 °C, by a Oxidative phosphorylation is dependent on proton motive force, and thermal vent (Mehta and Baross, 2006). The community both acidophiles and alkaliphiles have to deal with the composition in thermal environments are also impacted by pH, and extremes in external concentration and internal pH chemical species such as iron, sulfur, chloride, and (Pierson et al., (Krulwich et al., 1996). transport may be charge dependent 1999, Skirnisdottir et al., 2000; Inskeep and McDermott, 2005b; Inskeep and thus subject to the pH of the environment. Nevertheless, et al., 2007). microbial mats have been found to thrive in the extreme low pH of acid mine drainage (Bond et al., 2000a,b; Baker and Banfield, 2003) 2.3. Oxygen and acid sulfur springs (Meisinger et al., 2007), as well as the elevated pH of silicious hot springs (Nakagawa and Manabu, 2002; van der Flat laminated microbial mats are often the sites of steep oxygen Meer et al., 2000, 2005) and high pH (9–10) of alkaline lakes. To date, gradients that can transition from supersaturation (N500 μM), just the most extreme appears to be the microbial mats of Iron Mountain, below the sediment/water interface, to total anoxia within less than a with a pH of below 1 (Baker and Banfield, 2003). As might be millimeter (Dupraz and Visscher, 2005). of oxygen from the expected, the microbial diversity, based on 16S rRNA sequences, is quite limited to mostly species of Leptospirillum and Ferromicrobium (Bond et al., 2000b), with some Acidomicrobium and unidentified and Thermoplasmales as well (Bond et al., 2000a). Even in environments where the pH of the overlying water is near neutral, the metabolic activity of the different guilds can result in a pH gradient (Fig. 4). Oxygenic photosynthesis can raise the pH in excess of 9, while fermentation and can lower the pH to below 6.8 (Revsbech et al., 1983).

2.5. Salinity

The presence of dissolved soluble salts affects both the density and the chemical activity of water. The effect of salinity upon osmotic potential is particularly important from a biological perspective. Organisms living in marine and hypersaline environments are hypotonic with a cytoplasm less saline than the surrounding water. To counteract the tendency for water to leave the cell osmolites such as and glycine-betaine act as compatible solutes, creating an apparent osmotic potential equal to the external environment. Freshwater organisms are faced with the opposite problem. They are hypertonic and their cytoplasm is less dilute than their surroundings, thus water has a tendency to enter the cell. However, the difference is not as great as that facing marine organisms and water is regulated by active diffusion out of the cell. Most eukaryotic organisms can't handle either high salt or exposure to extreme oscillations in salinity. Thus flat laminated microbial mats often fl fl Fig. 4. Idealized profiles for oxygen, sulfide, and pH during the day (light) and night ourish in intertidal ats and hypersaline lagoons (Nicholson et al., (dark) (modified from Dupraz and Visscher, 2005). 1987; Stolz, 1990; Des Marais, 2003; Bachar et al., 2007). The tidal J. Franks, J.F. Stolz / Earth-Science Reviews 96 (2009) 163–172 167 changes in salinity that particularly occur in the affect 1983) but the accumulation of nitrate for later use in sulfide oxidation the microbial diversity, photosynthesis and respiration (Raeid et al., was documented only recently. 2007). There have been new discoveries about the ecological impact of alternative electron donors and acceptors. For example, arsenic is readily 2.6. Electron acceptors and donors, and chemical species cycled in hypersaline environments and in the absence of significant sulfate reduction, drives the ecology (Oremland et al., 2005a). More Microbial mats can be considered natural as they are recently, arsenic has been directly linked to photoautotrophy in biofilms often the site of intense biogeochemical cycling (Visscher and Stolz, from Mono Lake CA, with As(III) being used as an in the 2005). They can provide nitrogen and , and produce significant place of water or hydrogen sulfide (Kulp et al., 2008). Considering that amounts of H2 and CO, as well as methane (Pearl et al., 2000; Hoehler early microbial communities inhabited thermal and brine environ- et al., 2001). Energy generation and acquisition of essential elements ments, where arsenic should be abundant, one may speculate that these drive the transformation of chemical species. Thus the chemical systems were fueled in part by arsenic cycling. Indeed, active arsenic profile primarily reflects the metabolic activity of the guilds and cycling has been demonstrated for several mat communities assemblages, but is also influenced by abiotic factors. Energy and (Inskeep et al., 2007). The versatility of nitrate as a terminal electron carbon are provided by the autotrophic members of the community. acceptor has been expanded with the discovery of organisms that couple These include oxygenic photolithoautotophs (e.g., diatoms, cyano- nitrate reduction to the oxidation of sulfate (as described above), bacteria), anoxygenic photolithoautotrophs (e.g., purple sulfur arsenite (Oremland and Stolz, 2003), and ammonia, the latter being bacteria, green sulfur bacteria), anoxygenic photoorganotrophs known as “annamox” (Strous et al., 1999; Kuypers et al., 2003; Penton (e.g., , green filamentous bacteria), and chemo- et al., 2006). (e.g., iron oxidizing bacteria, sulfur oxidizing bac- teria, nitrifying bacteria, methylotrophs). The carbon in turn may be 3. Community structure oxidized back to CO2 through respiration (both aerobic and anaerobic) and fermentation. Respiration requires the availability Community structure is the species composition (occurrence and of electron acceptors, that in coupled reactions, oxidize the organics abundance) down the vertical profile defined within a network of (e.g., electron donors). The canonical progression of electron biogeochemical interactions. A microbial mat can be composed of acceptors, as predicted by thermodynamic considerations, is O2 → hundreds to thousands of species of organisms that are stratified into − +4 +3 −2 NO3 → Mn → Fe → SO4 → CO2. Thus one would expect the a number of layers (Cohen et al., 1977; Stolz, 1983; DesMarais et al., dominant process to proceed, from surface to depth, aerobic 1992; Ward et al., 1992; Castenholz, 1994; Ramsing et al., 2000; Stolz, respiration, nitrate reduction (e.g., denitrification), 2000, 2003). Primarily comprised of bacteria and some Archaea, reduction, iron reduction, sulfate reduction, then methanogenesis. eukaryotic organisms (e.g. diatoms) may also be significant (Bonny However, studies on flat laminated mats (Canfield and Des Marais, and Jones, 2007a,b). A variety of traditional techniques such as light 1991) and stromatolites (Visscher et al., 1998), have shown active and fluorescence microscopy, scanning and transmission electron sulfate reduction at or near the surface in the zone of oxygenic microscopy, have been used for species identification (Stolz, 1994, photosynthesis. In microbial ecosystems where light is not available Stolz et al., 2001). Flat laminated microbial mats are no different than (e.g., caves, deep sea), chemolithoautotrophy provides the bulk of the most of the other microbial systems, in that “99%” of the species are energy and carbon. Deep sea thermal vents and sulfur caves have unculturable. More recently culture independent methods (e.g., communities dominated by sulfur oxidizing epsilonproteobacteria molecular approaches discussed below) have been used to investigate (Engel et al., 2003, 2004; Alain et al., 2004; Nakagawa et al., 2005, (Jonkers et al., 2003; Martínez-Alonso et al., 2005; 2006). Cold methane seeps support communities of methylotrophs Baumgarter et al., 2006; Bachar et al., 2007). The microbial mats at and sulfur oxidizers (Michaelis et al., 2002; Reitner et al., 2005; Guerrero Negro, for example, generated more than 1500 16S rRNA Arakawa et al., 2006). Interestingly, the methane oxidation is an sequences representing over 750 species (Ley et al., 2006). Certain key anaerobic process and two groups of Archaea (ANME-1, ANME-2) species, especially phototrophs, can be readily identified in situ by have been identified that can couple the reduction of sulfate to the their ultrastructure (Stolz, 1983)(Fig. 3). Three examples of stratified oxidation of methane (Michaelis et al., 2002; Treude et al., 2003). The microbial communities are discussed below to demonstrate ecosys- Black Sea microbial mats were shown to simultaneously consume tem dynamics. methane and sulfate with the population dominated by ANME-1 type The sandy mat of the Great Sippewissett Marsh, Cape Cod, methylotrophs (Treude et al., 2005). More recently, the involvement Massachusetts is an example of a stratified microbial community of methyl sulfides in anaerobic methane oxidation has been reported (Nicholson et al., 1987). The mat is subject to the alternating tides, (Moran et al., 2008). Iron oxidizing chemolithoautotrophs support being submerged at high tide and exposed at low tide. Gradients of communities in both marine such as the iron-rich mats of the Loihi light, oxygen, and sulfide define the vertical profile. The community Seamount (Gao et al., 2006) and terrestrial such as Iron Mountain lies just below a surface layer of sand and has up to six layers (Bond et al., 2000a,b; Baker and Banfield, 2003). consisting of different microbial communities based on light and Microbial mats of filamentous chemolithoautotrophic sulfur- electron microscopy observations. These layers are discernable oxidizing bacteria (e.g., Beggiatoa spp., Thioploca spp., Thiomargarita because of the different populations of pigmented organisms. The namibiensis) have been found on surface sediments from coastal zones uppermost layer is in color due to the presence of diatoms and (e.g., Santa Barbara Basin), zones, cold seeps, methane a high concentration of carotenoids (Pierson et al., 1987). The next seeps, deep sea vents and mud (Mills et al., 2004; de Beer layer is green because of the presence of cyanobacteria such as Os- et al., 2006, Hinck et al., 2007; Preisler et al., 2007). The size of the cillatoria sp. and Lyngbya estuarii. The third layer is pink in color and is individual filaments may be quite large, as they can be up to 10 μmin populated by purple sulfur bacteria (e.g., Amoebobacter sp., Thiocapsa diameter and hundreds of microns in length (Gallardo and Espinoza, roseopersarcina). The oxygen concentration in the green layer is at 2007). Although known primarily for their ability to oxidize sulfide supersaturation because of active photosynthesis by the cyanobac- with oxygen, some species can store nitrate intracellularly (Jørgensen teria. The pink layer, however, is anoxic, due to the combination of and Gallardo, 1999; Schulz et al., 1999) and are capable of using nitrate high rates of respiration and sulfate reduction. The subsequent layers as the (Hinck et al., 2007). The diel migration of are also dominated by anoxygenic phototrophic bacteria (e.g., purple Beggiatoa and Thiovulum species in response to oxygen and sulfide and green phototrophic bacteria). The fourth layer is salmon in color gradients has been known for some time (Jørgensen and Revsbech, due to the presence of purple sulfur bacteria with bacteriochlorophyll 168 J. Franks, J.F. Stolz / Earth-Science Reviews 96 (2009) 163–172 b (e.g., Thiocapsa pfennigii). The olive or fifth layer is composed terrigenous sediment was also being reworked by heterotrophic primarily of the bacteriochlorophyll c containing green sulfur bacteria bacteria into a black ooze that reeked of hydrogen sulfide. After the (e.g., Prosthecochloris estuarii), and is underlain by a black, sulfurous third summer, M. cthonoplastes returned to dominate the surface layer. community. Initially there was a thick gelatinous surface layer contain- The above description is an oversimplification and may give the ing bundles of M. cthonoplastes, intermingled by filaments of S. subsalsa impression that these mat communities are a static system. Microbial and O. salina. Later a three layered mat developed. The yellow surface ecosystems are truly dynamic and can change dramatically over short layer was comprised mostly of diatoms (e.g., sp. Neitzche sp., time periods. These changes can be brought about by active motility as Rhopolodia sp.), but had bundles of M. cthonoplastes, of well as rapid growth. Microbes can cover great distances at speeds up Phormidium sp., O. salina,andS. subsalsa,aswellasclustersofApha- to hundreds of microns per propelled by flagella, gliding nothece sp., and Gleocapsa sp.. The second layer, green in color, was motility, or other means. There are purple sulfur bacteria in the pink dominated by the colonial coccoid . sp. and was layer of the Sippewissett sandy mat that have gas (Nicholson underlain by a black sulfurous mud. Although purple sulfur bacteria et al., 1987). Filaments of the sulfur oxidizing bacterium Beggiotoa sp., were observed, no distinct layer was formed. At this point, the formation are known to migrate several centimeters through sediment during of annual laminations resumed. It took almost four years, however, for the course of a night via gliding (Jørgensen and Revsbech, 1983; the full compliment of layers (yellow, green, , salmon, and black) to Moeller et al., 1985; Hinck et al., 2007). The growth of microorganisms reappear. Diatoms dominated the yellow layer, M. cthonoplastes and can also be a factor. With generation times as brief as 20 min, massive Chroococcidiopsis sp., the green layer, sp. and the green blooms of organisms can occur virtually overnight. bacterium Chloroflexus sp. in the red layer, and T. pfennigii in the salmon Catastrophic events in which a community or is close to layer. Still some species were missing. or completely destroyed eventually to recolonization. The These last two examples provide an interesting contrast even though phenomenon of succession in microbial ecosystems occurs in much they share similarities. The island of Mellum lies at 60° north latitude, the same way that has been described for terrestrial ecosystems. Two and the mats are seasonally destroyed. The communities are dominated studies on stratified microbial communities, one on Mellum Island in by rapid growing, upwardly mobile species and are reestablished every the North Sea, and the other in Laguna Figueroa, Baja California, year. Laguna Figueroa on the other hand, is in a subtropical climate, just Mexico, provide insight into how such succession occurs. above 30° north latitude. Although the flat laminated mats have an The island of Mellum is a small uninhabited island in the southern annual growing season, the community is usually not destroyed by the North Sea. Microbial mats are found in the upper intertidal zone and are spring high tides. Thus species with less tolerance for perturbation or especially well developed on the western shore. Three different mat slower growth kinetics may be able to persist. For this community, then, types have been described (Stal et al., 1985). The microbial community the periodic flooding and burial by terrestrial sediment has a greater in the newly colonized sand is comprised mostly of Oscillatoria sp. with impact on the community structure. The fact that a community is lesser populations of Spirulina sp. and coccoid cyanobacteria. Essentially, destroyed frequently does not necessarily mean the species diversity will this community begins to produce the organics and fix the nitrogen be any less, but rather that there is selective pressure for rapidly growing necessary to support a community of greater complexity. A more species. The mats of Great Sippewissett Marsh, like the ones of the island cohesive mat is dominated by the filamentous cyanobacterium Micro- of Mellum, are destroyed every winter and yet they develop into a coleus chthonoplastes. M. chthonoplastes is easily recognized by the multilayered community. This phenomenon is a reflection of the concept bundle of filaments in a common sheath. The third microbial mat type that organisms with short generation times can potentially respond to shows three layers, a surface green layer, dominated by filamentous environmental changes with expediency, whereas organisms with long cyanobacteria (M. chthonoplastes, Oscillatoria sp.), a red layer, dominated generation times may take a greater time to respond, but may also persist by purple sulfur bacteria (Thiocapsa sp., Thiopedia sp., Chromatium sp., long after the optimal conditions for their growth have disappeared. Ectothiorhodospira sp.), and an underlying black layer, indicative of the activity of sulfate reducing bacteria. The growing period for the mats 4. Advances in techniques begins in May or June and ends in October or November. During the winter they are often destroyed or greatly reduced in size. Growth The application of molecular approaches to the study of microbial begins again in the spring with the colonization of the pristine sand with ecology has revolutionized the field (Oremland et al., 2005b). Initial filaments of the nitrogen fixing Oscillatoria sp. (Stal et al., 1985). studies using dot blot hybridization and limited sequencing (Risatti et Laguna Figueroa is a small hypersaline lagoon on the PacificOcean al., 1994), have given way to large scale sequencing (Ward et al., 2006; side of Baja California, del Norte (Fig. 2). Several different mat types can Baumgartner et al., 2006), gene expression studies (Steunou et al., be found (Margulis et al., 1980; Stolz, 1990). Only those mats that are 2006), and metagenomic analysis (Bhaya et al., 2007). Volumes of 16S dominated by M. chthonoplastes, however, form laminations in the rRNA gene sequences are now available through NCBI (http://www.ncbi. sediment (Stolz, 1983; Stolz, 1990). Another distinguishing feature of nlm.nih.gov/) and the Ribosomal Database Project II (http://rdp.cme. this mat is that it has four distinct layers each representing different msu.edu/). Examples of phylogenetic studies based on 16S rRNA gene communities of phototrophic bacteria with : a surface sequences include intertidal mats (Rothrock and García-Pichel, 2005), yellow layer with mostly diatoms and the cyanobacteria Phormidium sp. hypersaline mats (Risatti et al., 1994; López-Cortéz et al., 2001; Nuebel and Aphanothece sp., a green layer with M. chthonoplastes and Chroo- et al., 2001; Casamayor et al., 2002; Jonkers et al., 2003; Sørenson et al., coccidiopsis sp., a red layer with anoxygenic filamentous purple bacteria 2005; Baumgartner et al., 2006), hot springs (Ruff-Roberts et al., 1994; (Chromatium sp., Thiocapsa roseoparsarcina)andaChloroflexus-like Ferris and Ward,1997; Ferris et al.,1997; Jackson et al., 2001; Ferris et al., organism, and a salmon layer with Thiocapsa (Stolz, 1990; Fig. 3). The 2003; Lacap et al., 2007; McGregor and Rasmussen, 2008), caves mats at Laguna Figueroa are usually only flooded for short periods each (Holmes et al., 2001; Engel et al., 2003, 2004), arctic hot springs spring. However, starting in 1979, corresponding with an unusually wet (Roeselers et al., 2007), Antarctic lake mats (Taton et al., 2003; Jungblut winter caused by a strong el Niño, the lagoon filled up with over 3 m of et al., 2005), benthic lakes (Koizumi et al., 2004), thermal vents (Alain fresh water and 10 cm of terrigenous sediment, virtually burying the et al., 2004; Nakagawa et al., 2005, 2006), methane seeps (Michaelis community. Although the previously deposited laminated sediment et al., 2002; Treude et al., 2003, 2005), and the microbial community remained intact, the microbial mat that formed them was destroyed. associated with (Barneah et al., 2007). These Once the receded, a thin veneer of halite covered the surface, studies have identified the major phylotypes and when done quantita- beneath which was a yellow layer of diatoms, and a thin green layer of tively, the dominant species. They have reinforced the idea that cyanobacteria (Oscillatoria salina, Spirulina subsalsa). The underlying microbial mats have great and are organized into J. Franks, J.F. Stolz / Earth-Science Reviews 96 (2009) 163–172 169 guilds and assemblages (Ward et al., 2006). The phylogenic analyses can gradient centrifugation. The 16S rRNA can then be amplified and also reveal historic features. The microbial community in Cuatro sequenced, and a species identification made (Schmid et al., 2006). Cienegas basin still maintains its marine heritage (50% of the phylotypes Fatty acid and pigment determination have also been useful tools for are more closely related to marine species) even though the organisms investigating community composition (Büehring et al., 2005; Nakajima have not seen seawater since the (Souza et al., 2006). et al., 2003). More recently, environmental has become a Conversely, amplification and sequencing of ribosomal genes from a rapidly evolving field. Based on the every increasing database of 217,000 year old Mediterranean sapropels identified phylotypes of sequences and their fingerprint (after trysin digest), protein freshwater green sulfur bacteria (Coolen and Overmann, 2007). Other fragments isolated from environmental samples can be identified using studies have probed for specific groups with targeted primers for 16S mass spectrometry (Maldi-TOF and MS-MS analysis) (Ram et al., 2005). rRNA genes (or the 16S–23S intergenic region, Leuko et al., 2007)or functional genes such as those involved in nitrogen fixation (Moisander 5. Summary et al., 2006), sulfate reduction (Dillon et al., 2007), and arsenite oxidase (Inskeep et al., 2007). In some cases the phylogeny obtained from the Any given environment, whether aquatic or terrestrial, may be functional genes parallels that of the 16S rRNA gene, such as the Fenner– defined by a set of physical properties and chemical characteristics. The Matthews–Olson protein in green sulfur bacteria (Alexander and Imhoff, physical properties are typically determined by abiotic processes while 2006). This approach, however, is not a panacea, as there are examples the chemical characteristics may be markedly affected by the activity of where the dominant phylotype has no known cultured relative. In organisms. The distribution of phototrophic bacteria is primarily addition, the techniques are dependent on proper sample collection and determined by light, oxygen, and hydrogen sulfide. The quantity and efficient nucleic acid extraction. Flash freezing is often used in sample quality of the light is affected by the light attenuating properties of collection, however, certain organisms readily lyse and their DNA is water, but also by absorption by the different types of phototrophic degraded in the process (Giacomazzi et al., 2005; Suomalainen et al., bacteria. The concentration of oxygen is affected by diffusion and mixing 2006), Conversely, some organisms are recalcitrant to cell lysis, and as well as production by oxygenic phototrophs. The concentration of nucleic acid extraction and amplification from natural samples can be sulfide is dependent on a source of sulfate, the activity of sulfate hampered by the chemical composition and presence of organics (as reducing bacteria, and sulfide diffusion and consumption. These reviewed in Bertrand et al., 2005; Desai and Madamwar, 2007). interactions result in dynamic systems that can exhibit both spatial Therefore, when characterizing a new community, a variety of methods and temporal heterogeneity, and provide a wide variety of environments should be tested, and the extraction efficiency determined. supporting a rich diversity of species. The application of culture There are now over 800 bacterial and 50 archaeal being independent methods including metagenomics, will provide new sequenced or completed. This information has facilitated the application insight into the community structure and dynamics of flat laminated of comparative (Klatt et al., 2007), functional gene arrays mats. Nevertheless, physiological and biochemical studies remain (Ward et al., 2007), and metagenomics (Ward et al., 2006; Wegley et al., essential for exploring the remarkable metabolic diversity and 2007) to probe functionality and diversity. In hot spring populations in of the microbial species that inhabit these important ecosystems. Spring (Yellowstone National Park), ecotypes of different Synecococcus have been recognized (Ward et al., 2006). M. chthono- Acknowledgements plastes that has been found in flat laminated mats across the globe are morphologically and ultrastructurally identical, but it is questionable This work was supported in part by NSF grant EAR 0221796. The whether they are all the same species or exhibit genetic variability and authors wish to thank the members of the Research Initiative for distinct depending on the environment. A recent study used Bahamian Stromatolites for fruitful discussions. RIBS contribution #45. three gene loci on strains of M. chthonoplastes isolated by micromani- pulation. The results seemed to indicate that there is indeed genetic References diversity in populations collected from the ten sites from three different locations investigated (Lodders et al., 2005). Use of sequence Alain, K., Zbinden, M., Le Bris, N., Lesongeur, F., Quérellou, J., Gaill, F., Cambon-Bonavita, M., 2004. Early steps in microbial colonization processes at deep-sea hydrothermal from pure cultures and metagenomic data from mixed populations will vents. Environ. Microbiol. 6, 227–241. allow for further investigation of the capabilities and interactions Alexander, B., Imhoff, J.F., 2006. 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