marine microbial thiotrophic ectosymbioses - HYDRA-Institute

2727_C04.fm Page 112 Wednesday, June 30, 2004 12:00 PM
112 J. Ott, M. Bright & S. Bulgheresi
Summary and outlook
The importance of the thiotrophic ectosymbioses varies greatly between the different cases. Fenchel
& Finlay (1989) calculated that the biomass of bacteria associated with specimens of Kentrophoros
in their sediments is only 3.7 ¥ 10 –4 g m –2 compared with a biomass of free-living sulphur-oxidising
bacteria of 5–20 g m –2 . It may therefore be merely “an exotic phenomenon which makes only a
symbolic contribution” (Fenchel & Finlay 1989). In Zoothamnium niveum it may be important at
a microspatial scale: with an estimated weight of the bacteria on an average colony of 1000
microzooids of 1 mg, the symbionts would contribute only 1.2 mg m –2 (assuming 1200 colonies;
Ott et al. 1998). Because the colonies are highly aggregated, this value increases 100-fold when
only the patches are taken into account (assuming 100 colonies on an area of 10 cm 2 ). In tropical
calcareous sands, where Stilbonematinae are a dominant element of the meiofauna (Ott & Novak
1989), the weight of the symbiotic bacteria may be in the same order of magnitude as that of freeliving
sulphur bacteria. At a density of about 300 ¥ 10 3 worms m –2 (consisting of equal numbers
of Laxus oneistus and Stilbonema majum, carrying on average half of the bacteria calculated for
an adult worm), the combined weight of the symbiotic bacteria would amount to 0.7–0.8 g. In the
case of Rimicaris the ectosymbionts are (with estimated 2.1–4.2 ¥ 10 11 bacterial cells m –2 ) significantly
more abundant than the sulphur-oxidising bacteria attached to the chimney surface (approximately
4.9 ¥ 10 8 m –2 ), but also dominate the water close to the chimney, which contains about 5
¥ 10 8 bacteria l –1 .
Sulphide symbioses are apparently a frequent outcome of the various associations of protists
and invertebrates with bacteria. The most common type of association leading to ectosymbioses is
fouling of surfaces, which originally involved a diversity of microbes, microalgae, and protists.
Evidence for this evolutionary intermediate stage is the many cases of irregular epigrowth reported
from ciliates, including relatives of Kentrophoros and Zoothamnium niveum, and nematodes that
are closely related to the Stilbonematinae. These fouled organisms may be regarded as models for
the ancestors of extant symbioses and apparently lack the ability to keep their surface free of
epibionts, which at high densities may become a nuisance (Ott 1996). This imperfection, however,
was a necessary precondition for the evolution of a successful mutualistic interaction. There is little
evidence pertaining to the age of thiotrophic symbioses. Most of the above-described hosts do not
fossilise well enough to leave an indication of bacterial symbioses. Only in the arthropods is there
some evidence that a microbial and possibly thiotrophic symbiosis existed in the Ordovician olenid
trilobites. These now extinct animals lived on reduced sediments, probably in dysoxic and sulphidic
bottom water. Their extended carapace has been interpreted as an incubation chamber for sulphur
bacteria, similar to that of Rimicaris (Fortey 2000).
The spectacular endosymbioses of the Vestimentifera and the large clams and mussels at hot
vents have directed much attention to these conspicuous animals. Until the discovery of the
Rimicaris symbiosis the study of ectosymbioses had not been pursued with the same effort. There
is, however, still much to discover both in shallow water and in the deep sea that will shed new
light on the fascinating functioning and evolution of thiotrophic symbioses.
References
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Allen, C.E. 1958. On the basic form and adaptations to the habitat in Lucinaceae (Eulamellibranchia).
Philosophical Transactions of the Royal Society of London Biological Sciences 241, 421–484.
Allen, C.E., Copley, J.T. & Tyler, P.A. 2001. Lipid partitioning in the hydrothermal vent shrimp Rimicaris
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