Stjepko Golubic

The Lithobiontic Ecological Niche, with Special Reference to Microorganisms

ABSTRACT Revised terminology is proposed that describes the ecological niches of microorganisms within hard, mineral substrates. Organisms attached to the external surfaces of the rock are termed epiliths, while those in the interior of the rock are all termed endoliths. The latter are called chasmoendoliths if they inhabit fissures in rocks, cryptoendoliths if they dwell within structural cavities, and euendoliths if they actively penetrate calcareous substrates.

Boring Microorganisms and Microborings in Carbonate Substrates

Boring or endolithic microorgani sms discussed herein are photosynthetic cyanophytes, eucary—otic green and red algae, and heterotrophic fungi that actively penetrate carbonate substrates. Although their existence has been known since the mid-nineteenth century, new techniques for preparation and study developed within the last decade have brought about significant progress in our understanding of them. Boring microorganisms have been studied in a variety of carbonate substrates, including the shells and skeletons of living organisms or their fragmented remains, and within coastal limestones.

Anatomy and taphonomy of a precambrian algal stromatolite

Abstract A single specimen of silicified flat algal stromatolite from the late Precambrian Bitter Springs Formation, Australia, contains three distinct microbial communities: (1) an entophysalidacean mat-building community comparable to both modern members of the genus Entophysalis and 2000 Ma old algae from the Belcher Islands, Canada; (2) a filamentous assemblage composed entirely of the Phormidium or Lyngbya-like cyanophyte Eomycetopsis; and (3) a non-stromatolitic assemblage of chroococcoid unicells that may have been associated with small, quickly evaporating ponds or puddles of water. Within each community, fossil preservation varies as a function of preservational microenvironments. Recognition of degradation sequences permits an assessment of taphonomic alterations of the original biological patterns. This, in turn, allows reconstruction of community associations and diversity patterns. The paleoenvironment of this particular Bitter Springs stromatolite is considered to be the lower part of the intertidal zone bordering a shallow, perhaps somewhat restricted sea. Post-mortem degradation has acted to increase apparent diversity through the creation of diagenetic variations in morphology and to decrease the same measure by the selective destruction of less resistant taxa. Three new species are described: Eoentophysalis cumulus, Eosynnechococcus amadeus, and Gloeodiniopsis gregaria.

Experimental studies on microbial bioerosion at Lee Stocking Island, Bahamas and One Tree Island, Great Barrier Reef, Australia: implications for paleoecological reconstructions

Different kinds of experimental calcareous substrates were exposed at Lee Stocking Island (Bahamas) and One Tree Island (Great Barrier Reef, Australia) to study which endolithic bacteria, algae and fungi contribute to bioerosion and what their bioerosion rates are. The sites at Lee Stocking Island were several leeward shallow water and several windward shallow and deep-water positions (from the Acropora palmata reef at 2 m down to 275 m depth). At One Tree Island, the experiments were conducted in patch reefs treated with P and N to study the influence of mineral nutrients on bioerosion. The exposure periods ranged from 1 week to 2 years. The micritic carbonate substrates exposed on Lee Stocking Island contained 6 genera with 15 species of cyanobacteria, green and red algae, and different kinds of microendolithic heterotrophs. The mean values of bioerosion rates measured between 1 to 2 g/m 2 /y at 275 m and 520 g/m 2 /y at one of the leeward sites. The composition of the endolithic community and the bioerosion rates changed over time. At One Tree Island, shell pieces of Tridacna were used as substrate exposed for 5 months to endolith activity. Five genera and 6 species of cyanobacteria, green and red algae and different kinds of heterotrophic microendoliths were found with bioerosion rates of 20–30 g/m 2 /y. There are differences in abundance of taxa between Lee Stocking Island and One Tree Island. The introduction of nutrients had no apparent impact on the microborer community. Controlling factors for the distribution and abundance of microborers are mainly light, but also the kind of substrate and, possibly, the biogeographic position. The results support the paleoecological importance of microendoliths.

Endolithic fungi in reef-building corals (Order : Scleractinia) are common, cosmopolitan, and potentially pathogenic

Reef-building corals appear to exist in dynamic equilibria with four principal partners: interconnected polyps of a colonial coelenterate, endosymbiotic dinoflagellate zooxanthellae residing in the host’s endoderm, endolithic algae that penetrate coral skeletons, and endolithic fungi that attack both endolithic algae and the polyps. Although reports of fungal and algal-like endoliths in corals date back almost 150 years (1) and evidence of a fossil history extends as far back as the Upper Devonian (;370 ma) (2), most attention has been paid to the structure (3), function (4, 5), and diversity (6) of the coral-zooxanthellae interactions, ignoring the endolithic members of the consortium. Recently, Le Campion-Alsumard et al. (1995) (7, 8) described an interrelationship between endolithic algae and fungi within the massive coral Porites lobata Dana 1846 (Poritidae), on Moorea island near Tahiti, French Polynesia. Fungi were also found to penetrate the most recently deposited skeletal material and to be associated with pearllike skeletal deposits formed by polyps of P. lobata in response to attack by their heterotrophic, endolithic symbionts. Here we extend these observations to the pocilloporid coral Pocillopora eydouxi and to the acroporid corals Acropora cytherea, Acropora humulis, and Montipora cf. studeri, collected at Johnston Atoll, central Pacific Ocean. Our observations suggest that direct coral-fungal interaction is widespread, not only geographically, but taxonomically as well. Thus, fungal endoliths, acting as opportunistic pathogens, may play a greater role in the ecology of coral reef systems than previously recognized. The oligophotic, siphonal green alga Ostreobium quekettii is ubiquitous in skeletons of live corals (9, 10). It is also common in other carbonate substrates, including dead shells and limestone, down to a depth of 300 m in clear waters of the Bahamas (11). Two other phototrophic organisms were reported from skeletons of live corals, the filamentous cyanobacterium Plectonema terebrans and conchocelis stages of bangiacean rhodophytes (12). Endolithic fungi in coral skeletons are equally common. They penetrate the corallum (euendolithic) and are often intermingled with endolithic algae, frequently parasitizing the latter (7). Fungi attack algal filaments by specialized hyphal branches, or haustoria, and often continue to grow inside algal filaments. Dense populations of algal and fungal endoliths have been associated with black-stained bands in specimens of P. lobata (13). Although skeletons of dead corals are bored by a variety of endolithic microorganisms, there has been no evidence that endoliths can penetrate the layer of tissue that covers living coral surfaces, leading to the conclusion that infestation by a limited number of specialized endoliths occurs early in the life of a coral, and that endolithic algae and fungi continue to grow in parallel with the accretion of the corallum (8). Most filaments of O. quekettii and endolithic fungi extend in the direction of the axes of skeletal growth. In P. lobata, borings were detected in newly deposited skeletal spines (pali), demonstrating that the endoliths are able to keep up with the rates of skeletal accretion (7, fig. 2). The pearl-like skeletal deposits are always associated with fungal attacks during the residence of polyps in actively growing calicies. The polyps encapsulate the advancing hypha into dense repair aragonite, forming a distinct skeletal structure referred to as a “cone” (7). The present study has two main objectives: to determine whether the relationship exhibited between P. lobata and endolithic fungi as described from the island of Moorea, in Received 7 July 1999; accepted 29 November 1999. *To whom correspondence should be addressed. E-mail: cbentis @bu.edu Reference: Biol. Bull. 198: 254–260. (April 2000)

Microbialites in a modern lagoonal environment: nature and distribution, Tikehau atoll (French Polynesia)

Abstract Microbialites, including stromatolitic structures, gelatinous masses and mats develop in Tikehau lagoon (Tuamotu, French Polynesia), on the flanks and slopes of numerous pinnacles and ‘motu’ islets between 0 and 25 m deep, on coral colonies, algal tufts or on lagoonal sediments. Individual stromatolitic structures consist of hemispherical domes and are produced by monospecific populations of filamentous cyanobacteria belonging to three distinctive Phormidium species, Symploca , and possibly to one new species of Schizothrix . Gelatinous masses hanging from the ceiling of caverns are produced by Phormidium laysanense . Microbial mats are well developed at all depths on pinnacle slopes and are produced by either monospecific or mixed cyanobacterial populations. The study of micro- and ultrastructure of stromatolites reveals that they result both from trapping and binding of sediments and from carbonate precipitation. In addition to phototrophic biomineralization, pervasive carbonate precipitation occurred in association with decaying organic matter. The basic constructional elements of the precipitated carbonate consist of 0.1–0.2-μm rounded bodies that form very fine anhedral to subhedral micrite; their surfaces comprise extremely small carbonate granules (20–50 nm). Gradual changes (ageing) in the ultrastructure of carbonate precipitates include the precipitation of successive euhedral calcite layers around these grains. Widespread development of microbialites in this pristine lagoonal environment results from rapid blooms of microbial benthic communities, possibly induced by temporary and local nutrient pulses. Nutrients seem to undergo a restricted circulation between the sediment and pinnacle reef frameworks. Pinnacles and reef islets are repeatedly affected by catastrophic storm events which cause redistribution of sediments and nutrients.

EARLY CYANOBACTERIAL FOSSIL RECORD : PRESERVATION, PALAEOENVIRONMENTS AND IDENTIFICATION

The cyanobacterial fossil record is among the oldest for any group of organisms, possibly reaching back to 3500 Ma ago. The molecular phylogeny of cyanobacteria is complementary to the fossil findings, confirming the antiquity of the group, the role of cyanobacteria in the evolution of planetary primary production, and the symbiotic origins of plastids in algae and plants from cyanobacterial ancestors. The study of fossil cyanobacteria followed the discovery of Precambrian microbial fossils by S.A Tyler and E.S. Barghoorn in 1954, and is still developing. Most fossil cyanobacteria are preserved in permineralized conditions in cherts and phosphorites or as organic compressions in shales. The interpretation of fossil cyanobacteria is aided by the study of modern counterparts, preferably within their natural habitats. These comparisons include the post mortem degradation of cellular remains. The fortuitous preservation and fossilization of ancient cyanobacterial communities in growth position, i.e. in the sy...

Desert crust formation and soil stabilization

Abstract A microbially formed soil cover known as desert crust carpets vast regions of land in the arid climates. An accretionary phenomenon in a generally erosional setting, it stabilizes soil and enhances its quality. It is potentially applicable to reclamation of unconsolidated soil in desert regions of the world. This paper reviews the work on microbial crusts, how they develop and contribute to soil quality, and what environmental variables enhance or impede their growth. Microbiological issues relating to the identification, isolation, and culturing of important members of this microbial community are discussed. Some practical problems are considered and suggestions for further research made.

Molecular and morphological characterization of cyanobacterial diversity in the stromatolites of Highborne Cay, Bahamas

Stromatolites are sedimentary deposits that are the direct result of interactions between microbes and their surrounding environment. Once dominant on ancient Earth, actively forming stromatolites now occur in just a few remote locations around the globe, such as the island of Highborne Cay, Bahamas. Although the stromatolites of Highborne Cay contain a wide range of metabolically diverse organisms, photosynthetic cyanobacteria are the driving force for stromatolite development. In this study, we complement previous morphological data by examining the cyanobacterial phylogenetic and physiological diversity of Highborne Cay stromatolites. Molecular analysis of both clone and culture libraries identified 33 distinct phylotypes within the stromatolites. Culture libraries exhibited several morphologically similar but genetically distinct ecotypes, which may contribute to ecosystem stability within the stromatolites. Several of the cultured isolates exhibited both a positive phototactic response and light-dependent extracellular polymeric secretions production, both of which are critical phenotypes for stromatolite accretion and development. The results of this study reveal that the genetic diversity of the cyanobacterial populations within the Highborne Cay stromatolites is far greater than previous estimates, indicating that the mechanisms of stromatolite formation and accretion may be more complex than had been previously assumed.

Cyanobacteria: Architects of Sedimentary Structures

Cyanobacteria, the oldest oxygenic phototrophs on the planet, once made the most significant impact on sediments and left an impressive fossil record of organo-sedimentary structures. Today, cyanobacteria dominate extreme environments where they participate in sediment production, construction and destruction, and leave characteristic, often species-specific, traces of their activities. Microbial ecosystems at the sediment-water interface are built and supported by cyanobacteria as the principal primary producers. Cyanobacterial photosynthesis promotes carbonate precipitation, delivering new sediment particles. Cyanobacterial growth, movement and behavioral responses often guide the depositional process and shape the resulting sedimentary structures. Conversely, cyanobacterial colonization and growth is also guided by changes in depositional environment. Cyanobacterial primary production at the sediment-water interface, coupled with rapid bacterial oxidation of this organic product, maintains steep redox gradients, creating additional metabolic niches. The consequent changes in mineral solubility promote biogeochemical cycling of elements and may lead to recrystallization and rearrangement of minerals. Destruction and alteration of sediments may be caused by cyanobacterial activities indirectly, or be carried out directly by euendolithic cyanobacteria which actively penetrate carbonate substrates. Evidence of both sediment-constructing and -destructing cyanobacterial behavior is found in carbonate deposits of the Mesoproterozoic age. As pioneer settlers on marine, freshwater and terrestrial sedimentary deposits, modern cyanobacteria prepare the ground for successive invasion and expansion of eukaryotic flora and fauna. In the historical context, and on a geological time scale, analogous sequences of events illustrate the evolutionary progression of life’s complexity, as cyanobacterially supported microbial ecosystems of marine and terrestrial environments gave way to eukaryote-dominated ones.