Coastal Microbial Mats: the Physiology of a Small-Scale Ecosystem

South Afllcan Journal of Botany 2001 67 399-410 CopYright © NfSC Ply Lid PrmtM m South Africa - AlIlIgllts roserved soutH AFRICAN jOURNAL OF BOTANY ISSN 0254-6299 Minireview Coastal microbial mats: the physiology of a small-scale ecosystem LJ Stal Netherlands Institute of Ecology, Centre for Estuarine and Marine Ecology, Department of Marine Microbiology, PO Box 140, NL -4400 AC Yerseke, Netherlands e-mail: stal @cemo.nioo.knaw.nl Received 10 May 2001, accepted in rev ised form 25 May 2001 Coastal inter-tidal sandy sediments! salt marshes and bacteria and the sulfide that they produce is oxidised by mangrove forests often support the development of anoxygenic phototrophic bacteria and by colorless SUl microbial mats. Microbial mats are complex associa fur bacteria. Growth and metabolism of these microor tions of one or several functional groups of microor ganisms result in markedly fluctuating vertical gradi ganisms and their formation usually starts with the ents of oxygen and sulfide that shift during a day-night growth of a cyanobacterial population on a solid sub cycle. This review discusses the metabolic contribu strate. They are considered as analogues of fossil tions of the different functional groups of microorgan Precambrian stromatolites. Primary production by the isms and how their joint effort results in the formation of cyanobacteria fuels the metabolism of sulfate reducing the mat. Introduction In their natural environment, microorganisms may occur matolites have been built th rough the growth and metabolic essentially in one of the following 3 ways: free-living. asso activity of microbial mals that lithilied through calcification ciated with an d often inside other organisms or fo rm ing mul and subsequently by silicification and other diagenetic ticellular, mono- or muftispecies aggregates. In the latter processes (Walter 1976). The lamination in the rock rep re form they may occur as colonies, biofilms or microbial mats. sents the seasonal or erratic growth pattern of the microbial I will not attempt to give an all-embracing definition of any of mats, comparable to the growth rin gs in the trunk of a tree . the 3 forms of microbial aggregates, because this seems to In stromatolites fossi l remnants of microorganisms have be a nearly impossible tas k and also the borderlines been found Ihat morphologically resemble modern between the diffe rent forms are in fact continuous. cyanobacteria, which also today are common builders of Nevertheless, it is important to indicate in a more general microbial mats (Schopf 2000) . Since there is little doubt that way of what is understood in Ihe framework of th is review by many of these stromatol ites were lormed through au totroph a microbial mat. Microorganisms th at grow on a solid sur ic metabolism, it is tempting to believe that they were built by face may eventually form microbial mats. Microbial mats cyanobacteria. However, the recent discovery that cyanobac have been the subject of 3 international meetings of which teria are an evolutionary relatively young group within the th e results have been published (Cohen et al. 1984, Cohen Proteobacteria, argues against this hypothesis (Gupta 2000). and Rosenberg 1989, Stal and Caumette 1994). A mat dif Modern microbial mats have been termed recent stroma fe rs fro m a biofilm mainly because of size and the coherent to li tes in order to distinguish them from th e fossil ones. structure typical for the former. In its ultimate form, microbial However, the majority of the modern microbial mats do not mats resemble something like a doormat, which can be lithify and therefore th e term 'stromatolite' was considered peeled from the surface as a whole. This explains the origin not appropriate, except in the few examples that are known of the concept of a microbial mat. Before this te rm became to calcify. The same is true for 'potential stromatolites' common property, microbial mats were known as 'laminated because it is uncertain whether non-calcifying microbial microbial ecosystems' or recent or potential stromatolites mats in fact possess the potential of lithification. Similar as (Krumbein 1983) . Stromatolites are fossil laminated rock for stromatolites, modern microbial mats retain a lamination, mations of biogenic origin . The oldest stromatolites date representing older, partly degrad ed mats. However, the term back to more than 3.5 Gyr B.P. and represent the earliest 'laminated microbial ecosystems' usually does not refer to indications of life on earth. It is generally accepted that stro- this historical lamination but rather to a vertical zonation of 400 Sial different functional groups of microorganisms , which is often colonise low-nutrient environments. In inter-tidal coastal visible to the naked eye because of the different colors. sediments they prefer fine sandy sediments , which combine Thus, the actual active microbial mat is laminated through moderately strong hydrodynamics and low sedimentation differen t groups of organisms. rales (Yallop et al. 1994). Moreover, the quartz sand grains However, neither the historical nor the instantaneous lam allow excellent Iransmission of lighl into Ihe sediments (Stal ination is the law of the Medes and Persians . Microbial mats , et al. 1985, Kuhl et al. 1994). Initial colonisation of the sedi after growlh has ceased, may be decomposed completely, ment by Ihe usually fi lamentous cyanobacte ria is Ihrough not leaving a visible trace and the substrate is co lonised adhesion to sand grains probably by sticky extracellular every season anew. Likewise, a microbial mat may be com polymers. This property allow cyanobacteria to colon ise posed of one species or different species may nol be sepa environments with relatively high energy, Without being rated into differenl strata or they may not be dislinguished as washed away. Some species are particularly well equipped such . Such systems are obviously not 'laminated' but Ihey to settle in high-energy environments. For instance, in the do nol principally differ from Ihe 'laminated microbial ecosys Bahama's Schizothrix spp. is known to colonise envi ron tems' and can all be em braced by the term 'microbial mat'. ments with strong wave currents where other organisms are Theorelically, microbial mats may be composed of one unable to sellie (Reid and Browne 1991 ). These organi sms particu lar species. However, as a ru le a complex microbial give rise to the formation of modern stromatolites. ecosystem forms, in which a variety of different functional groups of microorganisms rep resent a structu ral and physi Photorespiration ological unit (Van Gemerden 1993). II has been proposed that microbial mats are structural and physiological equiva Once a successful colonisation has occurred, the cyanobac lents of tissues (Wachendorfer 1991). teria th rough growlh and their pholosynlhetic aclivity enrich In this review I wi ll describe the processes and organisms the sediment with organic matter, which becomes available that are involved in Ihe formation of one Iype of microbial to other microorganisms. There are a number of different mal Ihat is buill by cyanobacteria Ihal is frequently found in mechanisms by which the pholosynthetically fixed carbon is coastal inteHida1 sediments, mangrove forests and salt liberated into the environment. An important mechanism marshes all around Ihe globe. Microbial mats developing in could be Ihrough pholorespiralion . The cyanobacterial mal extreme environments such as hypersaline ponds, thermal is characterised by a high concentration of biomass. The sp rings or hot or cold deserts, nor non-phototrophic systems oxygen thai is produced through pholosynthesis accumu such as mals of the gliding sulfur bacleri um Beggiatoa or lates in the mal and can only leave it through diffusion. Thioploca (Larkin and Strohl 1983) are nol discussed here. Although Ihe diffusion coefficienls of the polysaccharide matrix of the cyanobacterial mat is not much different from The de velopment of a cyanobacterial mat: primary pro that of water, the medium is stagnant and no turbulence can duction is the motor of the ecosystem aid the exchange of gas with the overlying water or air. Hence, the cyanobacterial mat may become supersaturated Colonisation with oxygen (Revsbech et al. 1983). Two to three-fold oxy gen supersaturation in cyanobacterial mats is not exception~ Inter-tidal sandy sediments are high energy environments , al. At the same time the inverse is true for C02. Carbon diox exposed to strong hydrodynamic conditions. Sediment parti ide is fixed during photosynthesis and depleted Irom Ihe cies of small grain size such as silt and cl ays will not deposit mat. It can only be repl enished by diffusion from the overly here , or they will be eroded away. On the most exposed ing medium . Rlbulose-l ,5-bisphosphale ca rboxylase/oxyge areas only the heavier quartz sand grains are deposited. nase (Rubisco) , the key enzyme of the reductive pen tose Inter-tidal sand flats can be consi dered as extreme environ phosphate cycl e (Calvin) an d Ihe enzyme responsible for ments because besides Ihe physical forces they are low in the fixation of CO.!, possesses also oxygenase activity, Le. nutrients and the periodic inundation causes desiccation and uses 0 2 for the oxidative cleavage of ribu l ose~ 1 ,5-bisphos· strong variations in salinity and temperature. Few organisms phate (Tabila 1994) . In facl, Rubisco has a much beller affin are capable of colon ising these environments. ily for 0 , than fo r CO, and in order 10 be able to effectively Cyanobacteria have remarkably few nutritional require fix CO" its concenlration musl be much higher Ihan 0 ,. In an ments. Their main way 01 life is photoautotrophic, which aerobic environment, many cyanobacteria (and other means Ihat they use light as the source of energy, water as microalgae) achieve th is requ irement by concentraling CO, the electron donor and C02 as the sole source 01 carbon (Carbon Concenlraling Mechanism, CCM) and Rubisco in (Stal 1995).

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