Occurrence and characteristics of unusual protistan symbionts from surgeonfishes (Acanthuridae) of the Great Barrier Reef, Australia

Clements, Kendall D.; Sutton, David C.; Choat, J. H.

doi:10.1007/bf00428493

Cited by 66 publications

(99 citation statements)

References 20 publications

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“…ruminants, herbivorous turtles and insects, manatees), most marine herbivorous fishes have a simple gut architecture and short retention times of a few hours or less (Lobe1 1981, Horn 1989) that appears to limit the importance of the gut microbiota. Of course, it should be noted that remarkable prokaryotic symbionts have been observed in the guts of several herbivorous and detritivorous acanthurids (Clements et al 1989, Clements & Bullivant 1991 and a unique gut architecture and anaerobic fermentation has been observed in 2 herbivorous kyphosids (Rimmer & Wiebe 1987). Though concentrations of acetate and propionate found in this study are comparable to those in other herbivores, short gut retention times may preclude a significant nutritional role for SCFA.…”

Section: Discussionsupporting

confidence: 48%

Herbivory by reef fishes and the production of dimethyl sulfide and acrylic acid

Dacey¹,

King²,

Lobel³

1994

Mar. Ecol. Prog. Ser.

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The content of dimethylsulfoniopropionate (DMSP) in selected marine reef macrophytes was examined and related to levels of DMSP and one of its decomposition products, dimethylsulfide (DMS), in guts of herbivorous fish. Concentrations of short-chain fatty acids and acrylic acid (ACR), another decomposition product of DMSP, were also measured in gut contents. The fatty acid data provide evidence for bacterial fermentation within fish intestines. Unlike previous observations of gut microflora, the concentrations of ACR in these guts did not support a role for ACR as an inhibitor of the gut microflora. DMSP also appears to concentrate in the tissues of certain fish, but not in others. These results illustrate the complex trophic interactions which determine the dynamics of DMSP in the marine food web.

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Section: Discussionsupporting

confidence: 48%

Herbivory by reef fishes and the production of dimethyl sulfide and acrylic acid

Dacey¹,

King²,

Lobel³

1994

Mar. Ecol. Prog. Ser.

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“…An individual fish often harbors multiple morphotypes and each Epulopiscium morphotype is found in multiple host species. Surgeonfish that harbor these symbiont populations are either herbivorous or detritivorous (primarily feeding on detritus) (14). None of the plankton-feeding surgeonfish species examined harbored Epulopiscium-like symbionts, nor did other herbivorous reef fish outside the surgeonfish family.…”

mentioning

confidence: 97%

“…The unusual morphology of these organisms, particularly with respect to their production of multiple intracellular offspring or daughter cells, warranted the description of a new genus and species, Epulopiscium fishelsoni (30). Subsequently, Clements and colleagues discovered a morphologically diverse group of Epulopiscium-like intestinal microorganisms in a variety of surgeonfish species from the South Pacific around the Great Barrier Reef (14).…”

mentioning

confidence: 99%

Nocturnal Production of Endospores in Natural Populations ofEpulopiscium-Like Surgeonfish Symbionts

et al. 2005

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Prior studies have described a morphologically diverse group of intestinal microorganisms associated with surgeonfish. Despite their diversity of form, 16S rRNA gene surveys and fluorescent in situ hybridizations indicate that these bacteria are low-G؉C gram-positive bacteria related to Epulopiscium spp. Many of these bacteria exhibit an unusual mode of reproduction, developing multiple offspring intracellularly. Previous reports have suggested that some Epulopiscium-like symbionts produce dormant or phase-bright intracellular offspring. Close relatives of Epulopiscium, such as Metabacterium polyspora and Clostridium lentocellum, are endospore-forming bacteria, which raises the possibility that the phase-bright offspring are endospores. Structural evidence and the presence of dipicolinic acid demonstrate that phase-bright offspring of Epulopiscium-like bacteria are true endospores. In addition, endospores are formed as part of the normal daily life cycle of these bacteria. In the populations studied, mature endospores were seen only at night and the majority of cells in a given population produced one or two endospores per mother cell. Phylogenetic analyses confirmed the close relationship between the endospore-forming surgeonfish symbionts characterized here and previously described Epulopiscium spp. The broad distribution of endospore formation among the Epulopiscium phylogenetic group raises the possibility that sporulation is a characteristic of the group. We speculate that spore formation in Epulopiscium-like symbionts may be important for dispersal and may also enhance survival in the changing conditions of the fish intestinal tract.

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“…reproduce by the internal production of multiple offspring referred to as daughter cells (8,16,27). Daughter cells are initiated in the tips of an Epulopiscium cell and grow until they completely fill the parental cell (16,27).…”

mentioning

confidence: 99%

Phylogenetic analysis of Metabacterium polyspora: clues to the evolutionary origin of daughter cell production in Epulopiscium species, the largest bacteria

1996

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It is rare that there are molecular clues to the evolutionary origin of developmental traits. We have encountered an evolutionary juxtaposition that may explain the origin of the unique replicative morphology of Epulopiscium spp., the largest known bacteria, which reproduce by the internal production of multiple live offspring. We report here a 16S rRNA-based phylogenetic analysis of Metabacterium polyspora, a multipleendospore-forming, uncultivated inhabitant of guinea pig cecum. Cells of M. polyspora were harvested from cecum contents by sedimentation in a Ficoll gradient and lysed. The bacterial 16S rRNA genes of this lysate were amplified by PCR. Sequence analysis of the cloned PCR products revealed two dominant, closely related 16S rRNA types. In situ hybridization of cecum contents with fluorescently labeled oligonucleotides, diagnostic of these two sequences, showed that they represent distinct strains of M. polyspora. Phylogenetic analyses of the sequences showed that M. polyspora is closely related to Epulopiscium spp. On the basis of this result and other correlations, we propose that the process of sporulation was modified in a predecessor of Epulopiscium spp. to produce live offspring instead of quiescent endospores.

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Occurrence and characteristics of unusual protistan symbionts from surgeonfishes (Acanthuridae) of the Great Barrier Reef, Australia

Cited by 66 publications

References 20 publications

Herbivory by reef fishes and the production of dimethyl sulfide and acrylic acid

Herbivory by reef fishes and the production of dimethyl sulfide and acrylic acid

Nocturnal Production of Endospores in Natural Populations ofEpulopiscium-Like Surgeonfish Symbionts

Phylogenetic analysis of Metabacterium polyspora: clues to the evolutionary origin of daughter cell production in Epulopiscium species, the largest bacteria

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