Polymeric substances and biofilms as biomarkers in terrestrial materials: Implications for extraterrestrial samples

Organic polymeric substances are a fundamental component of microbial biofilms. Microorganisms, especially bacteria, secrete extracellular polymeric substances (EPS) to form slime layers in which they reproduce. In the sedimentary environment, biofilms commonly contain the products of degraded bacteria as well as allochthonous and autochthonous mineral components. They are complex structures which serve as protection for the colonies of microorganisms living in them and also act as nutrient traps. Biofilms are almost ubiquitous wherever there is an interface and moisture (liquid/liquid, liquid/solid, liquid/gas, solid/gas). In sedimentary rocks they are commonly recognized as stromatolites. We also discuss the distinction between bacterial biofilms and prebiotic films. The EPS and cell components of the microbial biofilms contain many cation chelation sites which are implicated in the mineralization of the films. EPS, biofilms, and their related components thus have strong preservation potential in the rock record. Fossilized microbial polymeric substances (FPS) and biofilms appear to retain the same morphological characteristics as the unfossilized material and have been recognized in rock formations dating back to the Early Archaean (3.5 b.y.). We describe FPS and biofilms from hot spring, deep-sea, volcanic lake, and shallow marine/littoral environments ranging up to 3.5 b.y. in age. FPS and biofilms are more commonly observed than fossil bacteria themselves, especially in the older part of the terrestrial record. The widespread distribution of microbial biofilms and their great survival potential makes their fossilized remains a useful biomarker as a proxy for life with obvious application to the search for life in extraterrestrial materials.

[1]  C. Allen,et al.  Microscopic physical biomarkers in carbonate hot springs: implications in the search for life on Mars. , 2000, Icarus.

[2]  A. Steele,et al.  An atomic force microscopy study of the biodeterioration of stainless steel in the presence of bacterial biofilms , 1994 .

[3]  J. Oehler.  Experimental studies in Precambrian paleontology: Structural and chemical changes in blue-green algae during simulated fossilization in synthetic chert , 1976 .

[4]  E. Buffetaut,et al.  Morphogenetic impact of microbial mats on surface structures of Kimmeridgian micritic limestones (Cerin, France) , 1991 .

[5]  R. Castenholz.  Microbial mat research: The recent past and new perspectives , 1994 .

[6]  F. Prahl,et al.  Early Diagenesis: Consequences for Applications of Molecular Biomarkers , 1993 .

[7]  W. G. Characklis,et al.  Seasonal variations in bacterial colonisation of stainless steel, aluminium and polycarbonate surfaces in a sea water flow system , 1989 .

[8]  W. S. Fyfe,et al.  Metal Interactions with Microbial Biofilms in Acidic and Neutral pH Environments , 1989, Applied and environmental microbiology.

[9]  K. Cooksey,et al.  Biofilms and microbial fouling , 1983 .

[10]  H. Chafetz,et al.  Bacterially Induced Lithification of Microbial Mats , 1992 .

[11]  Norman R. Pace,et al.  Origin of life-facing up to the physical setting , 1991, Cell.

[12]  R. Clark,et al.  Detection of crystalline hematite mineralization on Mars by the Thermal Emission Spectrometer: Evide , 2000 .

[13]  M. Fletcher,et al.  Bubble Contact Angle Method for Evaluating Substratum Interfacial Characteristics and Its Relevance to Bacterial Attachment , 1982, Applied and environmental microbiology.

[14]  L. Margulis,et al.  Reassessment of roles of oxygen and ultraviolet light in Precambrian evolution , 1976, Nature.

[15]  J W Costerton,et al.  How bacteria stick. , 1978, Scientific American.

[16]  F. Westall,et al.  A study of fossil microstructures from the Eocene Messel Formation using Transmission Electron Microscopy , 1996 .

[17]  G. Geesey,et al.  Interactions between metal ions and capsular polymers , 1989 .

[18]  J. Schopf,et al.  Microfossils of the Early Archean Apex Chert: New Evidence of the Antiquity of Life , 1993, Science.

[19]  R. Zare,et al.  Search for Past Life on Mars: Possible Relic Biogenic Activity in Martian Meteorite ALH84001 , 1996, Science.

[20]  J. Schopf,et al.  Early Archean (3.3-billion to 3.5-billion-year-old) microfossils from Warrawoona Group, Australia. , 1987, Science.

[21]  M. Walsh,et al.  Microfossils and possible microfossils from the Early Archean Onverwacht Group, Barberton Mountain Land, South Africa. , 1992, Precambrian research.

[22]  Wolfgang E. Krumbein,et al.  Stromatolites—the Challenge of a Term in Space and Time , 1983 .

[23]  Roger E. Summons,et al.  2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis , 1999, Nature.

[24]  E S Barghoorn,et al.  Microorganisms from the Gunflint Chert: These structurally preserved Precambrian fossils from Ontario are the most ancient organisms known. , 1965, Science.

[25]  J. Schopf,et al.  Artificial Microfossils: Experimental Studies of Permineralization of Blue-Green Algae in Silica , 1971, Science.

[26]  T. Beveridge,et al.  Metal Ions and Bacteria , 1989 .

[27]  G. Geesey,et al.  Isolation and partial chemical analysis of firmly bound exopolysaccharide from adherent cells of a freshwater sediment bacterium. , 1985, Canadian journal of microbiology.

[28]  Zbigniew Lewandowski,et al.  Effects of biofilm structures on oxygen distribution and mass transport , 1994, Biotechnology and bioengineering.

[29]  Andrew H. Knoll,et al.  Exceptional preservation of photosynthetic organisms in silicified carbonates and silicified peats , 1985 .

[30]  M. Alexander,et al.  Nonbiodegradable and other racalcitrant molecules , 1973 .

[31]  J. Glover.  Sediments of Early Archaean coastal plains : a possible environment for the origin of life , 1992 .

[32]  C. Défarge,et al.  Kopara in Polynesian atolls: early stages of formation of calcareous stromatolites , 1994 .

[33]  T. Parker,et al.  Transitional morphology in West Deuteronilus Mensae, Mars: Implications for modification of the lowland/upland boundary , 1989 .

[34]  L. Margulis,et al.  On the experimental silicification of microorganisms. III. Implications of the preservation of the green prokaryotic alga prochloron and other coccoids for interpretation of the microbial fossil record , 1978 .

[35]  Frances Westall,et al.  The nature of fossil bacteria: A guide to the search for extraterrestrial life , 1999 .

[36]  G. Bock,et al.  Evolution of hydrothermal ecosystems on Earth (and Mars , 1998 .

[37]  J. Banfield,et al.  Microbial extracellular polysaccharides and plagioclase dissolution , 1999 .

[38]  R Buick,et al.  Archean molecular fossils and the early rise of eukaryotes. , 1999, Science.

[39]  B. Jakosky,et al.  The biological potential of Mars, the early Earth, and Europa. , 1998, Journal of geophysical research.

[40]  M. Fletcher.  The Measurement of Bacterial Attachment to Surfaces in Static Systems , 1992 .

[41]  E. Shock,et al.  High-temperature life without photosynthesis as a model for Mars. , 1997, Journal of geophysical research.

[42]  M. Walsh,et al.  Filamentous microfossils from the 3,500-Myr-old Onverwacht Group, Barberton Mountain Land, South Africa , 1985, Nature.

[43]  W. S. Fyfe,et al.  Metallic ion binding by Bacillus subtilis; implications for the fossilization of microorganisms , 1988 .

[44]  L. Margulis,et al.  On the Experiemntal Silicification of Microorganisms. I. Microbial Growth on Organosilicon Compounds , 1977 .

[45]  H. Yanagawa,et al.  Thermophilic microspheres of peptide-like polymers and silicates formed at 250°C , 1985 .

[46]  S. Giovannoni,et al.  The microbial community in the layered sediments at Laguna Figueroa, Baja California, Mexico: Does it have Precambrian analogues? , 1980 .

[47]  C. Largeau,et al.  A Review of Macromolecular Organic Compounds That Comprise Living Organisms and Their Role in Kerogen, Coal, and Petroleum Formation , 1993 .

[48]  C. Turley,et al.  Microbial response to the input of fresh detritus to the deep-sea bed , 1990 .

[49]  Frances Westall,et al.  Electron microscope methods in the search for the earliest life forms on Earth (in 3.5-3.3 Ga cherts from the Barberton greenstone belt, South Africa): applications for extraterrestrial life studies , 1998, Optics & Photonics.

[50]  L. Margulis,et al.  On the experimental silicification of microorganisms II. On the time of appearance of eukaryotic organisms in the fossil record , 1978 .

[51]  F. Westall,et al.  Biofilms, microbial mats and microbe-particle interactions: electron microscope observations from diatomaceous sediments , 1994 .

[52]  R. Summons,et al.  Molecular fossils and microfossils of prokaryotes and protists from Proterozoic sediments , 1990 .

[53]  J. Lawless,et al.  Thermal Synthesis of Amino Acids from a Simulated Primitive Atmosphere , 1973, Nature.

[54]  S. Altobelli,et al.  Experimental and conceptual studies on mass transport in biofilms , 1995 .

[55]  C. Reimers,et al.  Role of bacterial mats in oxygen-deficient marine basins and coastal upwelling regimes: Preliminary report , 1983 .

[56]  David C. Pieri,et al.  Coastal Geomorphology of the Martian northern plains , 1993 .

[57]  S. Fox,et al.  Ancient microspheres: abiogenic, protobiogenic, or biogenic? , 1983 .

[58]  B. Simoneit,et al.  Lipid biomarkers for bacterial ecosystems: studies of cultured organisms, hydrothermal environments and ancient sediments. , 1996, Ciba Foundation symposium.

[59]  S. Awramik.  Chapter 6.3 Gunflint Stromatolites: Microfossil Distribution in Relation to Stromatolite Morphology , 1976 .

[60]  G. Geesey,et al.  Extracellular polymers for metal binding , 1990 .

[61]  J. Farmer,et al.  Fossilization processes in siliceous thermal springs: trends in preservation along thermal gradients. , 1996, Ciba Foundation symposium.

[62]  R. D. Hon,et al.  Martian lake basins and lacustrine plains , 1992 .

[63]  I. Sutherland,et al.  Uptake of metals by bacterial polysaccharides , 1993 .

[64]  H. Chafetz,et al.  Preservation of Microbes in Geyserite and Siliceous Sinter: Yellowstone National Park, Wyoming , 1999 .