Abstract
Sulfur-oxidizing chemoautotrophic (thioautotrophic) bacteria are now known to occur as endosymbionts in phylogenetically diverse bivalve hosts found in a wide variety of marine environments. The evolutionary origins of these symbioses, however, have remained obscure. Comparative 16S rRNA sequence analysis was used to investigate whether thioautotrophic endosymbionts are monophyletic or polyphyletic in origin and to assess whether phylogenetic relationships inferred among these symbionts reflect those inferred among their hosts. 16S rRNA gene sequences determined for endosymbionts from nine newly examined bivalve species from three families (Vesicomyidae, Lucinidae, and Solemyidae) were compared with previously published 16S rRNA sequences of thioautotrophic symbionts and free-living bacteria. Distance and parsimony methods were used to infer phylogenetic relationships among these bacteria. All newly examined symbionts fall within the gamma subdivision of the Proteobacteria, in clusters containing previously examined symbiotic thioautotrophs. The closest free-living relatives of these symbionts are bacteria of the genus Thiomicrospira. Symbionts of the bivalve superfamily Lucinacea and the family Vesicomyidae each form distinct monophyletic lineages which are strongly supported by bootstrap analysis, demonstrating that host phylogenies inferred from morphological and fossil evidence are congruent with phylogenies inferred for their respective symbionts by molecular sequence analysis. The observed congruence between host and symbiont phylogenies indicates shared evolutionary history of hosts and symbiont lineages and suggests an ancient origin for these symbioses.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allen JA (1958) On the basic form and adaptations to habitat in the Lucinacea (Eulamellibranchia). Philos Trans R Soc (Ser B) 684:421–482
Bernard FR (1974) The genus Calyptogena British Columbia with a description of a new species. Venus 33:11–22
Boss KJ (1970) Fimbria and its lucinoid affinities (Mollusca; Bivalvia). Breviora 350:1–16
Brooks DR (1988) Macroevolutionary comparisons of host and parasite phylogenies. Ann Rev Ecol Syst 19:235–259
Campbell KA (1992) Recognition of a Mio-Pliocene cold seep setting from the northeast Pacific Convergent Margin, Washington, U.S.A. Palaios 7:422–433
Cavanaugh CM (1985) Symbiosis of chemoautotrophic bacteria and marine invertebrates from hydrothermal vents and reducing sediments. Biol Soc Wash Bull 6:373–388
Cavanaugh CM (1993) Microbial symbiosis: patterns of diversity in the marine environment. Am Zool, in press
CoBabe EA (1991) Lucinid bivalve evolution and the detection of chemosynthesis in the fossil record. PhD thesis, Harvard University, Cambridge, MA
Cunningham CW, Buss LW, Anderson C (1991) Molecular and geologic evidence of shared history between hermit crabs and the symbiotic genus Hydractinia. Evolution 45:1301–1316
Distel DL, Delong EF, Waterbury JB (1991) Phylogenetic characterization and in situ localization of the bacterial symbiont of shipworms (Teredinidae: Bivalvia) by using 16S rRNA sequence analysis and oligonucleotide probe hybridization. Appl Environ Microbiol 57:2376–2382
Distel DL, Felbeck H (1988) Pathways of inorganic carbon fixation in the endosymbiont bearing lucinid clam Lucinoma aequizonata: part 1. Purification and characterization of the endosymbiotic bacteria. J Exp Zool 247:1–10
Distel DL, Lane DJ, Olsen GJ, Giovannoni SJ, Pace B, Pace NR, Stahl DA, Felbeck H (1988) Sulfur-oxidizing bacterial endosymbionts: analysis of phylogeny and specificity by 16S rRNA sequences. J Bacteriol 170:2506–2510
Distel DL, Wood AP (1992) Characterization of the gill symbiont of Thyasira flexuosa (Thyasiridae: Bivalvia) by use of polymerase chain reaction and 16S rRNA sequence analysis. J Bacteriol 174: 6317–6320
Eisen JA, Smith SW, Cavanaugh CM (1992) Phylogenetic relationships of chemoamotrophic bacterial symbionts of Solemya velum Say (Mollusca: Bivalvia) determined by 16S rRNA gene sequence analysis. J Bacteriol 174:3416–3421
Felbeck H, Distel DL (1992) Prokaryotic symbionts in marine invertebrates. In: Ballows A, Trüper H, Harder W, Schleifer KH (eds) The Prokaryotes. Springer-Verlag, New York, pp 3891–3906
Felsenstein J (1989) Phylip-Phylogeny inference package. Cladistics 5:164–166
Fiala-Médioni A, Felbeck H (1990) Autotrophic processes in invertebrate nutrition: bacterial symbiosis in bivalve molluscs. Comp Physiol 5:49–69
Fisher CR (1990) Chemoautotrophic and methanotrophic symbioses in marine invertebrates. Rev Aquat Sci 2:399–436
Goedert JL, Squires RL (1993) First oligocene records of Calyptogena (Bivalvia: Vesicomyidae). Veliger 36:72–77
Grey MW (1989) Origin and evolution of mitochondrial DNA. Ann Rev Cell Biol 5:25–50
Haygood MG, Distel DK (1993) Bioluminescent symbionts of flashlight fishes and deep-sea anglerfishes form unique lineages related to Vibrios. Nature 363:154–156
Haygood MG, Distel DL, Herring PJ (1992) Polymerase chain reaction and 16S rRNA gene sequences from the luminous bacterial symbionts of two deep-sea anglerfishes. J Mar Biel Assoc UK 72: 149–159
Hultman T, Stahl S, Hornes E, Uhlen M (1989) Direct solid phase sequencing of genomic and plasmid DNA using magnetic beads as solid support. Nucleic Acids Res 17:4937–4946
Lane DJ (1991) 26S/23S sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. John Wiley and Sons, New York, 115–175
Lane DJ, Harrison AP, Stahl D, Pace B, Giovannoni SJ, Olsen GJ, Pace NR (1992) Evolutionary relationships among sulfur- and iron-oxidizing eubacteria. J Bacteriol 174:269–278
MacDonell MT, Colwell RR (1985) Phylogeny of the Vibrionaceae, and recommendation for two new genera, Listonella and Schewanella. Syst Appl Microbiol 6:171–182
Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning. Cold Spring Harbor Laboratories, Cold Spring Harbor
Margulis L, Fester R (1991) Symbiosis as a source of evolutionary innovation. The MIT Press, Cambridge, MA
McAlester AL (1966) Systematics, affinities and life habits of Babinka, a transitional Ordovician lucinoid bivalve. Paleontology 8:231–246
McFall-Ngai MJ, Ruby EG (1992) Symbiont recognition and subsequent morphogenesis as early events in an animal-bacterium mutualism. Science 254:1491–1494
Munson MA, Baumann P, Clark MA, Baumann L, Moran NA, Voegtlin DJ, Campbell BC (1991) Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J Bact 173:6321–6324
Newell ND (1969) Classification of Bivalvia. In: Treatise on invertebrate paleontology. The Geological Society of America and The University of Kansas, vol 1, pp N205-N224
Olsen GJ, Overbeck R, Larson N, Marsh TL, McCaughey MJ, Maciukenas MA, Kuan WM, Macke TJ, Xing Y, Woese CR (1992) Ribosomal database project. NAR (20) supplement: 2199–2200
Pojeta J Jr. (1971) Review of Ordovician pelecypods. US Geol Survey Prof Paper 695:46
Pojeta J Jr. (1978) The origin and early taxonomic diversification of pelecypods. Philos Trans R Soc Lend B 284:225–243
Purchon RD (1987) Classification and evolution of the bivalvia: an analytical study. Philos Trans R Soc Lond B316:277–302
Reid RGB, Brand DG (1986) Sulfide-oxidizing symbiosis in Lucinaceans: implications for bivalve evolution. Veliger 29:3–24
Rowan R, Powers DA (1991) A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science 251:1348–1350
Ruby EG, Jannasch HW (1982) Physiological characteristics of Thiomicrospira sp. strain L-12 isolated from deep-sea hydrothermal vents. J Bacteriol 149:161–165
Ruby EG, Wirsen CO, Jannasch HW (1981) Chemolithotrophic sulfur-oxidizing bacteria from the Galapagos rift hydrothermal vents. Appl Environ Microbiol 42:317–324
Smith CR, Kukert H, Wheatcroft RA, Jumars PA, Deming JW (1989) Vent fauna on whale remains. Nature 341:27–28
Smith SW, Overbeek R, Olsen G, Woese C, Gillevet PM, Gilbert W (1992) Genetic data environment and the Harvard genome database. In: Genome mapping and sequencing, May 6–10. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, p 190
Squires RL, Goedert JL (1991) New late Eocene mollusks from localized limestone deposits formed by subduction-related methane seeps, southwestern Washington. J Paleontol 65:412–416
Stackebrandt E, Murray RGE, Trüper HG (1988) Proteobacteria classis nov., a name for the phylogenetic taxon that includes the purple bacteria and their relatives. Int J Syst Bacteriol 40:213–216
Stahl DA, Lane DJ, Olsen GJ, Pace NR (1984) Analysis of hydrothermal vent-associated symbionts by ribosomal RNA sequences. Science 224:409–411
Turner RD (1985) Notes on mollusks of deep-sea vents and reducing sediments. Am Malacol Bull 1:23–24
Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271
Wood AP, Kelly DP (1993) Reclassification of Thiobacillus thyasiris as Thiomicrospira thyasirae comb. nov., an organism exhibiting pleomorphism in response to environmental conditions. Arch Microbiol 159:45–47
Zharkikh A, Li WH (1992) Statistical properties of bootstrap estimation of phylogenetic variability from nucleotide sequences. I. Four taxa with a molecular clock. Mol Biol Evol 9:1119–1147:543–546
Author information
Authors and Affiliations
Additional information
Correspondence to: D.L. Distel
Rights and permissions
About this article
Cite this article
Distel, D.L., Felbeck, H. & Cavanaugh, C.M. Evidence for phylogenetic congruence among sulfur-oxidizing chemoautotrophic bacterial endosymbionts and their bivalve hosts. J Mol Evol 38, 533–542 (1994). https://doi.org/10.1007/BF00178852
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00178852