Olav Giere

Endosymbiotic sulphate-reducing and sulphide-oxidizing bacteria in an oligochaete worm

Stable associations of more than one species of symbiont within a single host cell or tissue are assumed to be rare in metazoans because competition for space and resources between symbionts can be detrimental to the host. In animals with multiple endosymbionts, such as mussels from deep-sea hydrothermal vents and reef-building corals, the costs of competition between the symbionts are outweighed by the ecological and physiological flexibility gained by the hosts. A further option for the coexistence of multiple symbionts within a host is if these benefit directly from one another, but such symbioses have not been previously described. Here we show that in the gutless marine oligochaete Olavius algarvensis, endosymbiotic sulphate-reducing bacteria produce sulphide that can serve as an energy source for sulphide-oxidizing symbionts of the host. Thus, these symbionts do not compete for resources but rather share a mutalistic relationship with each other in an endosymbiotic sulphur cycle, in addition to their symbiotic relationship with the oligochaete host.

Survival in an extreme habitat: the roles of behaviour and energy limitation

Extreme habitats challenge animals with highly adverse conditions, like extreme temperatures or toxic substances. In this paper, we report of a fish (Poecilia mexicana) inhabiting a limestone cave in Mexico. Several springs inside the cave are rich in toxic H2S. We demonstrate that a behavioural adaptation, aquatic surface respiration (ASR), allows for the survival of P. mexicana in this extreme, sulphidic habitat. Without the possibility to perform ASR, the survival rate of P. mexicana was low even at comparatively low H2S concentrations. Furthermore, we show that food limitation affects the survival of P. mexicana pointing to energetically costly physiological adaptations to detoxify H2S.

Structure and position of bacterial endosymbionts in the gill filaments of lucinidae from bermuda (Mollusca, Bivalvia)

SummaryThe gills of four lucinid bivalves from fine sediments in shallow reaches of Bermuda, Anodontia philippiana, Lucina multilineata, L. radians, and L. costata, were observed by electron microscope. They harbour intracellular bacterial endosymbionts similar to those in gills of clams from hydrothermal vents and other ‘sulphide biotopes’. The bacteria-containing bacteriocytes are found in distinct positions in the gill filaments, alternating with cells not invaded by the prokaryotes but with abundant mitochondria. Referring to the specific environment of the collected bivalves and to literature data from corresponding studies, the significance of this bacteria/animal association is discussed.

Ecology and biology of marine oligochaeta — an inventory rather than another review

Instead of updating the1982-review by Giere & Pfannkuche, it was deemed more useful to highlight some recent and relevant studies given the limited number of new and pertinent publications. In addition, new data on population ecology, some recent results on symbiotic associations and descriptions of adaptations to oxygen deficiency and hydrogen sulfide will be commented on. The scarcity of new ecological and biological studies on marine Oligochaeta, an animal group that often attains key positions in important shore areas, is alarming. Future research efforts on this ecologically relevant annelid group are seriously needed.

Structural peculiarities of the body wall of Tubificoides benedii (Oligochaeta) and possible relations to its life in sulphidic sediments

SummaryTubificoides benedii [=Peloscolex benedeni] a ubiquitous tubificid from poorly oxygenated, often polluted coastal muds, is known to be exceptionally well adapted to sulphidic sediments. However, almost nothing is known about its structural peculiarities, such as the conspicuously papillate body surface and possible relations to its unusual ecology. As a consequence, a study of this abundant but extraordinary marine worm has been made with the use of light and electron microscopy. While many internal structures correspond to the general pattern of marine tubificids and are not mentioned here, the epidermis — cuticle complex is unusual. The thick cuticle forms numerous high leaf-shaped papillae covered by condensed, almost solid mucus caps. The intermediate furrows usually harbour many different bacteria embedded in mucus. This mucus cover is rich in precipitates containing sulphur and other xenobiotic substances. Together with the cuticular papillae it can be sloughed off in a “moulting process”. Epicuticular projections, usually typical of oligochaetes, are absent from most parts of the body except from the first and last segments. The epidermal cells often contain numerous extremely long and abnormally shaped mitochondria. The significance of the peculiar structure of the body wall and the distinct “moulting” are discussed in the light of the ecological situation of these tubificids.

Tubificoides benedii (Tubificidae, Oligochaeta) — a pioneer in hypoxic and sulfidic environments. An overview of adaptive pathways

Eutrophic tidal flats and polluted coastal sites are the predominant habitat of the marine oligochaete Tubificoides benedii. The worms live in dense populations in these stressed habitats which are often characterized by high levels of hydrogen sulfide. This indicates that they have a high capacity to tolerate anoxic (and sulfidic) conditions. Respiration rates of T. benedii measured at various oxygen concentrations showed that aerobic respiration is maintained even at very low oxygen concentrations. This ability is combined with a high regulatory capacity of oxygen uptake. Addition of sulfide considerably reduced this capacity of maintaining aerobic metabolic pathways at low oxygen concentrations. The present work in relation to earlier physiological and structural studies (Giere et al, 1988; Dubilier et al., 1994, 1995, 1997) suggests adaptive strategies that make T. benedii one of the most successful inhabitants of ecologically stressed, sulfidic benthic environments. This is corroborated by comparison with other typical’ sulfide annelids’ such as the polychaetes Capitella capitata and Arenicola marina.

A systematic account of the Questidae (Annelida, Polychaeta), with description of new taxa

Questidae is a poorly known polychaete family with many unusual characters, particularly with regard to its reproductive organs. Its taxonomic position remains uncertain, which can be partly referred to the limited material described to date. New material, mostly from shallow sublittoral sediments, shows that questids have a circummundane distribution. Questa Hartman, 1966 is revised to include Novaquesta Hobson, 1970 as a junior synonym. Eight species of questids are assigned to Questa, four of them are new to science: Questa bicirrata sp. n., Q. paucibranchiata sp. n., Q. mediterranea sp. n., and Q. riseri sp. n. Character patterns of the questid polychaetes described so far are cladistically analysed. The limitation of informative characters causes ambiguity in the most parsimonious reconstruction of the phylogeny of the family, and therefore, the Questidae is proposed to be classified as comprising only one genus.

The gutless oligochaete Phallodrilus leukodermatus Giere, a tubificid of structural, ecological and physiological relevance

Phallodrilus leukodermatus is not only characterized by the complete absence of mouth, gut, anus and nephridia, but also by an exceptional dermal ultrastructure which is associated with gram-negative bacteria. The vertical distribution of the worms from Bermudian carbonate sands is also unusual in attaining population maximum at oligoxic or anoxic depths around the redox discontinuity (RPD) layer, where extremely high concentrations of amino acids and sugars are to be recorded. Based on results from current ecophysiological and ultrastructural studies, an interpretation of the unique biology of the worms is attempted.

The Bacterial Endosymbiosis of the Gutless Nematode, Astomonema Southwardorum : Ultrastructural Aspects

The recently described gutless Astomonema southwardorum Austen, Warwick & Ryan 1993, from North Sea methane seeps lives in symbiosis with oval, extracellular bacteria completely filling the lumen of a modified gut. The bacterial strand is tightly lined by a thin layer representing very long intestinal cells of the host. The bacteria are 5.5–6.0 µm in maximum length and 3.5–4.0 µm in width. In the anterior body the alimentary tract is completely reduced. The structure and size of the symbiotic prokaryotes, as well as their extracellular location in the lumen of a non-functional gut, differ substantially from those in A. jenneri , the single species of this genus thoroughly studied electron-microscopically (Ott et al., 1982). These structural discrepancies suggest a careful reassessment of the genus Astomonema .

Taxonomy and new bacterial symbioses of gutless marine Tubificidae (Annelida, Oligochaeta) from the Island of Elba (Italy)

Abstract In shallow sublittoral sediments of the north-west coast of the Island of Elba, Italy, a new gutless marine oligochaete, Olavius ilvae n. sp., was found together with a congeneric but not closely related species, O. algarvensis Giere et al., 1998. In diagnostic features of the genital organs, the new species differs from other Olavius species in having bipartite atria and very long, often folded spermathecae, but lacking penial chaetae. The Elba form of O. algarvensis has some structural differences from the original type described from the Algarve coast (Portugal). The two species from Elba share characteristics not previously reported for gutless oligochaetes: the lumen of the body cavity is unusually constricted and often filled with chloragocytes, and the symbiotic bacteria are often enclosed in vacuoles of the epidermal cells. Regarding the bacterial ultrastructure, the species share three similar morphotypes as symbionts; additionally, in O. algarvensis a rare fourth type was found. The divergence of the symbioses in O. algarvensis, and the coincidence in structural and bacteria-symbiotic features between the two taxonomically different, but syntopic host species at Elba are discussed.