In the beginning: egg–microbe interactions and consequences for animal hosts

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Abstract

Microorganisms are associated with the eggs of many animals. For some hosts, the egg serves as the ideal environment for the vertical transmission of beneficial symbionts between generations, while some bacteria use the egg to parasitize their hosts. In a number of animal groups, egg microbiomes often perform other essential functions. The eggs of aquatic and some terrestrial animals are especially susceptible to fouling and disease since they are exposed to high densities of microorganisms. To overcome this challenge, some hosts form beneficial associations with microorganisms, directly incorporating microbes and/or microbial products on or in their eggs to inhibit pathogens and biofouling. Other functional roles for egg-associated microbiomes are hypothesized to involve oxygen and nutrient acquisition. Although some egg-associated microbiomes are correlated with increased host fitness and are essential for successful development, the mechanisms that lead to such outcomes are often not well understood. This review article will discuss different functions of egg microbiomes and how these associations have influenced the biology and evolution of animal hosts.

This article is part of the theme issue ‘The role of the microbiome in host evolution’.

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OXYGEN TRANSPORT IN EGG MASSES OF THE AMPHIBIANS RANA SYLVATICA AND AMBYSTOMA MACULATUM: CONVECTION, DIFFUSION AND OXYGEN PRODUCTION BY ALGAE

Friet, SE Pinder (1994)

Many amphibians lay their eggs in gelatinous masses up to 1020 cm in diameter, posing problems for diffusive oxygen delivery. Oxygen may also be provided by water convection between eggs or by oxygen production by endogenous algae. We studied egg masses of two local amphibians, Rana sylvatica and Ambystoma maculatum, to estimate the importance of each of these processes. We injected dye to check for water channels, measured oxygen partial pressures within egg masses to determine the influence of external water convection and lighting, measured oxygen consumption and production in darkness and light and calculated expected gradients through egg masses with a cylindrical, homogeneous egg mass model. Rana sylvatica had relatively loose egg masses with water channels between the eggs; water convection was important for oxygen delivery. Ambystoma maculatum had firm egg masses with no spaces in the jelly between eggs; thus, there was no opportunity for convective oxygen delivery. The egg masses were cohabited by Oophila ambystomatis, a green alga found specifically in association with amphibian egg masses. Oxygen delivery in A. maculatum was by diffusion and by local production by the algal symbiont. Analysis of a cylindrical egg mass model and measurement of oxygen gradients through egg masses indicated that diffusion alone was not adequate to deliver sufficient O2 to the innermost embryos at late developmental stages. In the light, however, egg masses had a net oxygen production and became hyperoxic. Over the course of a day with a 14 h:10 h light:dark cycle, the innermost embryos were alternately exposed to hyperoxia and near anoxia.

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Transmission of a bacterial consortium in Eisenia fetida egg capsules.

Rebecca K Davidson, Peter D. Stahl, Theresa Powell (2010)

The earthworm Eisenia fetida harbours Verminephrobacter eiseniae within their excretory nephridia. This symbiont is transferred from the parent into the egg capsules where the cells are acquired by the developing earthworm in a series of recruitment steps. Previous studies defined V. eiseniae as the most abundant cell type in the egg capsules, leaving approximately 30% of the bacteria unidentified and of unknown origin. The study presented here used terminal restriction fragment length polymorphism analysis together with cloning and sequencing of 16S rRNA genes to define the composition of the bacterial consortium in E. fetida egg capsules from early to late development. Newly formed capsules of E. fetida contained three bacterial types, a novel Microbacteriaceae member, a Flexibacteriaceae member and the previously described V. eiseniae. Fluorescent in situ hybridization (FISH) using specific and general rRNA probes demonstrated that the bacteria are abundant during early development, colonize the embryo and appear in the adult nephridia. As the capsules mature, Herbaspirillum spp. become abundant although they were not detected within the adult worm. These divergent taxa could serve distinct functions in both the adult earthworm and in the egg capsule to influence the competitive ability of earthworms within the soil community. © 2010 Society for Applied Microbiology and Blackwell Publishing Ltd.