- Citado por SciELO
- Citado por Google
- Similares en SciELO
- Similares en Google
versión impresa ISSN 0717-652Xversión On-line ISSN 0717-6538
Gayana (Concepc.) v.70 supl.1 Concepción oct. 2006
Suplemento Gayana 70: 22-25, 2006
The sediment microorganisms under the oxygen minimum zone: present day analogs of precambrian oceans?
Los microorganismos de sedimentos bajo la zona de mínimo oxigeno: análogos de oceanos precambricos?
Victor Ariel Gallardo & Carola Espinoza
Department of Oceanography and Center for Oceanographic Research in the Eastern South Pacific (FONDAP-COPAS), P.O. Box 160-C, University of Concepcion, Concepcion, Chile, email@example.com
A review of the latest findings relating big filamentous sublittoral bacteria of sediments under the oxygen minimum zone (OMZ) of the eastern Pacific, and, on the basis of associated morphological and environmental factors, an analysis and comparison of extant and Precambrian similar benthic microorganisms is performed. Based on the similarity between the two communities and the fact that certain features presented by extant bacterial mats may explain a special type of Precambrian stromatolites, i.e., the microbialites, we suggest that both extant big filamentous bacteria and their mats may represent analogs of those existing in Precambrian oceans providing opportunities for research and clues on the evolution of early life in the ocean's shelf sediments and that this `forgotten biosphere' will eventually contribute to a better understanding of the biodiversity of present day's microbial world.
Keywords: Sediment bacteria, big bacteria, microfossils, Precambrian, Proterozoic, stromatolites, microbialites, bacterial mats.
Se revisan los últimos hallazgos sobre las grandes bacterias filamentosas habitantes del sublittoral bajo la zona de mínimo oxígeno (ZMO) del Pacífico oriental, y, sobre la base de la morfología y factores ambientales asociados se realiza un análisis de similares microorganismos actuales y Precámbricos. Basados en la similitud entre las dos comunidades y el hecho que ciertas características de los tapices bacterianos presentes podrían explicar un tipo especial de estromatolito precámbrico, i.e., los microbialitos, sugerimos que tanto las actuales bacterias filamentosas como sus tapices representan análogos de aquellos que existieron en el Precámbrico abriendo oportunidades para la investigación y pistas acerca de la evolución de la vida temprana en los sedimentos de la plataforma continental de los océanos.
Palabras Claves: Bacterias en sedimentos, grandes bacterias, microfósiles, precámbrico, proterozoico, estromatolitos, microbialitos, tapices bacterianos.
The sediments of the Oxygen Minimum Zone of the eastern South Pacific were the first to render massive populations of large, free-living, microorganisms reported as `cyanophyceae' in 1963 (Gallardo 1963, 1966). It took a little longer to realize that those massive findings of large filamentous forms were actually bacteria of the genus Thioploca (Gallardo 1977a). Two vacuolated marine species were later described, the first of the genus to be reported from the marine environment which may or not be found living freely or occupying a gelatinous sheath (Maier & Gallardo 1984). Today this genus is classified among the Gamma Proteobacteria (Teske et al. 1996). The size of their trichomes ranges from ca. 15-45 mm in diameter and from a few hundred microns to several centimeters and thus we call them `megabacteria'. Their occurrence was suggested for other similar oceanographic settings (Gallardo 1977b) and this forecast has proven true with findings in several localities along the OMZ of the eastern Pacific OMZ and in sediments under the OMZ off Namibia in the Benguela Current Ecosystem (Gallardo et al. 1998).
THE NEW MACROBACTERIA
Recently, however, a new system of microorganisms consisting again of predominantly big filamentous morphotypes, was discovered in the same Thioploca mat under summer OMZ conditions off Concepcion, central Chile (Gallardo & Espinoza in prep.) and has been confirmed in other shelf localities along the eastern Pacific with records so far from two sites off northern Chile (Mejillones and Iquique), two off Peru (Bahia Independencia and Callao), and one off Costa Rica (Golfo Dulce). The size of these new forms is smaller than those of the Thioploca and Thioploca-like trichomes ranging from less than one to a few micrometers in diameter and from a few tenths to several millimeters in length, thus our naming them `macrobacteria'. These forms are normally non-vacuolated but also in the recent observations, vacuolated, spherical Thiomargarita and Thiomargarita-like forms have shown up albeit of more modest sizes, i.e., ca. 60 um, than the originally described ones from Namibia.
While the sheathed mat-building Thioploca spp. are adapted to make a living by bridging over the near-bottom, nitrate-rich, suboxic water and the inner sedimentary, sulfide-rich, anoxic layer, there is some evidence to suggest that the newly observed macrobacteria may be facultative or obligate anaerobes living entirely within the sediment interstitial water of the reduced silt and clay particles (Espinoza, Nielsen & Gallardo, in prep.), i.e., sharing the biotope with the anaerobic meiobenthos (small metazoans, Nematoda in particular). Other microbes, in particular Protista (forams, ciliates and flagellates) also contribute to build the mat. No doubt the community contains also the ubiquitous regular `microbacteria', and perhaps even `nannobacteria'.. It should be emphasized that at the latitude of central Chile, it is during the spring and summer that the combined populations of mega- and macrobacteria constitute well defined mats which have been the subject of visual underwater observations with interesting results that will be discussed below.
Different techniques than those used for the regular bacteria are needed for the study of both the mega- and the macrobacteria, e.g., some can easily be micromanipulated and isolated and, initially, their distinct morphologies and behaviors can be observed, microphotographed and filmed under simple optical contrast-phase microscopy. More advanced optical techniques would of course render more useful information. Obviously the determination of the phylogeny and physiology of the components of this new ecosystem is one of the largest challenges marine microbiology faces today.
THE FORGOTTEN `BIOSPHERE'
We will call this, the `forgotten biosphere', because not only they have been overlooked by decades of research but also because many like forms have been described in the paleobiological literature, but unrecognized as potential sublittoral bacteria. On the first count, as the result of a review of the big bacteria, where the marine, cylindrical, multicellular, Beggiatoa spp. and Thioploca spp., and the spherical Thiomargarita namibiensis were analyzed, the authors asked themselves "why are there not more physiological types of bacteria that have developed large size to break the thermodynamic limitations of microscale?" and finally concluded that an open mind should be kept toward the potential extremes of prokaryotes, because "it is likely that we can await many more surprises from the enigmatic world of big bacteria."
This premonitory statement came to reality sooner than expected and prompted a literature search that lead to the conclusion that, beyond those scientific efforts relating the above genera, there were two major areas of research in which `mega' - and `macrobacteria', in particular, filamentous macrobacteria, were dealt with, i.e., the paleobiological area and the area of the engineering of waste-water treatment! (See: http://www.environmentalleverage.com/). We will mostly deal with the first area which connects with the ocean environment.
PRECAMBRIAN FILAMENTOUS BACTERIA
Indeed, many filamentous forms, dating from about 3.5 Ga ago, had been described in the paleobiological literature since the middle of last century (fide Schopf & Blacic 1971). Up to 1992 close to 100 species (with genus and specific Latin names) of filamentous (besides many spherical) forms had been recognized from the various fossil-bearing rocks around the world, some as old as the Archaean (Schopf 1968, Schopf & Klein 1992). Some of these fossil microorganisms resemble extant filamentous cyanobacteria and, probably, not having other reference, that is why most of them were assigned to that group, including those that originated an oxygenated atmosphere (Schopf & Blacic 1971). Conversely, the mats produced by extant cyanobacteria have been likened to stromatolite formations so abundant in Precambrian fossil-bearing beds. Judging from the analysis of the published photographic record, we posit however that, at least some of the fossil morphs, could actually be Thioploca-like sulfur bacteria and some of the stromatolite types might have been the produce of Thioploca-type bacterial mats, including the above mentioned `macrobacteria". Furthermore, it will be shown that some filamentous fossil forms resemble some of the recently discovered macrobacteria and still others (bearing full Latin names of genus and species) may instead be the fossilized form of empty sheaths of filamentous Thioploca-like sulfide bacteria.
EXTANT BACTERIA AND THEIR MATS AS ANALOGS OF THOSE PRECAMBRIAN
Because the earliest widespread occurrence of shelf-type sediments dates back to about 2.5 Ga, (Schopf 1975) i.e., the lower one third of the Proterozoic era, with oxygen conditions probably similar to those of the OMZ of today (Canfield & Teske 1996), it shouldn't be surprising to find fossil bacterial morphotypes similar to those still present today under similar conditions of suboxia or anoxia (Canfield et al. 2000, Anbar & Knoll 2002). We will present the analysis of published information on filamentous microfossils and its comparison with similar analysis performed on extant morphotypes as found under the OMZ off the eastern South Pacific. We will discuss the morphological dichotomies presented by the set of large benthic marine microbes, and as far as possible, physiological, ecological and oceanographic aspects to arrive at the suggestion that these newly found forms may be descendants/analogs of those that lived in shelf sediments of Precambrian oceans. We will also discuss the possibility that some morphological features produced by the microbial mats under study off central Chile might explain a particular type of Late Archean fenestrate stromatolites, namely the cuspate, net-like, and tented `microbialites' (Sumner 2000). With all this in mind we suggest that both extant big filamentous bacteria and their mats may represent analogs of those existing in Precambrian oceans providing opportunities for research and clues on the evolution of early life in the ocean's shelf sediments and that this `forgotten biosphere' will eventually contribute to a better understanding of the biodiversity of present day's microbial world, a picture that is continuously changing (Sogin et al. 2006).
This is a contribution of the Department of Oceanography and the Center for Oceanographic Research in the Eastern South Pacific Project #15010007). Thanks are extended to all those persons, including many students, and institutions that have contributed in so many ways along the many years of study of this fascinating oxygen deficient system where so much there is still to be discovered.
Anbar, A.D. & A. Knoll. 2002. Proterozoic ocean chemistry and evolution: a bioinorganic bridge. Science 297:1137-1142. [ Links ]
Canfield, D. & A. Teske. 1996. Late Proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulfur-isotope studies. Nature 382:127-132. [ Links ]
Canfield, D. et al. 2000. The Archean sulfur cycle and the early history of atmospheric oxygen. Science 658-661. [ Links ]
Gallardo, V.A. 1963. Notas sobre la densidad de la fauna bentónica en el sublittoral del norte de Chile. Gayana (Zool.) 10:3-15. [ Links ]
Gallardo, V.A. 1976. On the benthic sulfide system on the continental shelf of north and central Chile, p. 113-117. In J.C. Valle (ed.). Proceedings of the International Symposium of Coastal Upwelling, Universidad del Norte, Centro de Investigaciones Submarinas, CIS, Coquimbo, Chile. [ Links ]
Gallardo, V.A. 1977a. Large benthic microbial communities in sulphide biota under Peru-Chile Subsurface Countercurrent. Nature (London) 268:331-332. [ Links ]
Gallardo, V.A. 1977b. On the discovery of a large microbial community living in the bottoms of the continental shelf off Chile and Peru. An. Inst. Invest. Mar. Punta Betin, Santa Marta, Colombia 1:23-29. [ Links ]
Gallardo, V.A., E. Klingelhoffer, W. Arntz & M. Graco. 1998. First report of the bacterium Thioploca in the Benguela ecosystem off Namibia. J. Mar. Biol. Ass. U. K., 78:1007-1010. [ Links ]
Maier, S. & V.A. Gallardo. 1984. Thioploca araucae sp. nov. and Thioploca chileae sp. nov. Int. J. Syst. Bacteriology 34:414-418. [ Links ]
Schopf, J.W. 1968. Microflora of the Bitter Springs Formation, Late Precambrian, central Australia. J. Paleontology 42(3):651-688. [ Links ]
Schopf, J.W. 1975. Precambrian paleobiology: problems and perspectives. Annu. Rev. Earth Planet. Sci. 3:213-249. [ Links ]
Schopf, J.W. 1992. Atlas of representative Proterozoic microfossils. Pp. 1055-1117. In J.W. Schopf & C. Klein (eds.) "The Proterozoic Biosphere: A Multidisciplinary Study". Cambridge Univ. Press, Cambridge. [ Links ]
Schopf, J.W. & C. Blacic. 1971. New microorganisms from the Bitter Spring Formation (Late Precambrian) of the north-central Amadeus Basin, Australia. J. Paleontology 45(6):925-959. [ Links ]
Schopf, J.W. & C. Klein. 1992. The Proterozoic Biosphere. Cambridge University Press. [ Links ]
Sogin, M.L., H.G. Morrison, J.A. Huber, D.M. Welch, S.M. Huse, P.R. Neal, J.M. Arrieta & G.J. Herndl. 2006. Microbial diversity in the deep sea and the underexplored "rare biosphere". PNAS. [ Links ]
Sumner, D.Y. 2000. Microbial vs environmental influences on the morphology of Late Archean fenestrate microbialites. Pp. 307-314. In R.E. Riding & S.M. Awramik (eds.). Microbial Sediments. Springer-Verlag, Berlin, Heidelberg, New York. [ Links ]
Teske, A.P., N.B. Ramsing, J. Kuever & H. Fossing. 1995. Phylogeny of Thioploca and related filamentous sulfide-oxidizing bacteria. Syst. Appl. Microbiol. 18:517-526. [ Links ]