Further Development 24.7.2: How Do Symbionts Get Together?

Development and the Environment: Biotic, Abiotic, and Symbiotic Regulation of Development

All symbiotic associations must meet the challenge of maintaining their partnerships over successive generations. In the well-known associations between bacteria and metazoans, a bacterial symbiont must somehow become intimately associated with its metazoan host. There are three major ways that this is accomplished.

The first involves external transfer. Here, the metazoan host is born free of bacterial symbionts and becomes infected from the environment. This appears to be the case in squid infections with Vibrio fischeri. A squid is born without these bacteria and acquires them from the water. Nyholm and colleagues (2000) have shown that a newborn squids secrete a sticky viscous material from the pores of the presumptive light organ and produce water currents that direct bacteria from the seawater onto these regions. Once on this sticky matrix, the symbiotic bacteria can migrate into the pores and into the light organs. The second way is through horizontal transfer. Here, the hosts are born free of symbionts, but they acquire them from members of the parental generation. The third way, vertical transfer, involves gametes (most commonly, the oocyte) that carry the symbionts to the next generation.

Several types of vertical transmission mechanisms have been observed (Krueger et al. 1996). Females of the oligochaete worms Inanidrilus leukodermatus and I. planus appear to infect their offspring by smearing symbionts onto their own eggs. This occurs as the eggs pass through symbiont-coated genital pads of the mother as they leave her body (Giere et al. 1991). Certain clams (such as Solemya reidiSolemya velum, and Calyptogena soyae) produce oocytes that contain the microbial symbionts in their cytoplasm. Polymerase chain reaction techniques and electron microscopy have been used to find bacterial symbionts in the host ovaries, eggs, and larvae (Endow and Ohta 1990; Cary 1994; Krueger et al. 1996).

A preliminary report (Geilenkirchen et al. 1971) suggests a fascinating way that certain symbionts can get into the larval gut as the gut is forming. Dentalium eggs appear to be infected with their gut symbionts from the ovarian cells of their mothers. These symbionts adhere to the developing egg, specifically at the vegetal pole. During early cleavage, these bacteria are seen on the polar lobe during its first and second extrusions, and in later cleavage, they are observed on the descendents of the D blastomere. The microbes appear to be carried into the gut by the 4D or 4d blastomere as it enters into the embryo. From there, they are able to obtain residence in the gut and ovary.

Symbiotic relationships call into question the notion of individuality. Neither "organism" can survive alone, only as a composite. Similarly, developmental symbioses are calling into question the notion that animals develop as independent units. In many instances, it takes a community to raise an embryo.

Literature Cited

I would like to thank Ms. Megan Streams for bringing these papers to my attention.

Cary, S. C. 1994. Vertical transmission of a chemoautotrophic symbiont in the protobranch bivalve, Solemya reidiMol. Marine Biol. Biotech. 3: 121-130.

Endow, K. and Ohta, S. 1990. Occurence of bacteria in the primary oocytes of the vesicomyid clam Calyptogena soyaeMar. Ecol. Prog. Ser. 64: 309-311.

Geilenkirchen, W. L. M., Timmermans, L. P. M., Dongen, C. A. M., and Arnolds, W. J. A. 1971. Symbiosis of bacteria with eggs of Dentalium at the vegetal pole. Exper. Cell Res. 67: 477-478.

Giere, O., Conway, N. W., Gastrock, G., and Schmidt, C. 1991. "Regulation" of gutless annelid ecology by endosymbiotic bacteria. Mar. Ecol. Prog. Ser. 68: 287-299.

Krueger, D. M., Gustafson, R. G., and Cavanaugh, C. M. 1996. Vertical transmission of chemoautotrophic symbionts in the bivalve Solemya velum (Bivalvia: Protobranchia ). Biol. Bull. 190: 195-202.

Nyholm, S. V. Stabb, E. V., Ruby, E. G., and McFall-Ngai, M. J. 2000. Establishment of an animal-bacterial association: Recruiting symbiotic vibrios from the environment. Proc. Natl. Acad. Sci. USA 97: 10231-10235.




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