期刊论文详细信息
BMC Evolutionary Biology
Temporal variation and lack of host specificity among bacterial endosymbionts of Osedax bone worms (Polychaeta: Siboglinidae)
Robert C Vrijenhoek1  Rahel M Salathé2 
[1] Monterey Bay Aquarium Research Institute, Moss Landing, CA, 95039, USA;Present Address: Department of Biology and Center of Infectious Disease Dynamics, The Pennsylvania State University, Millennium Science Complex, University Park, PA, 16801, USA
关键词: Endosymbionts;    Oceanospirillales;    Ribotyping;    16S rRNA;    Osedax;   
Others  :  1140240
DOI  :  10.1186/1471-2148-12-189
 received in 2012-03-09, accepted in 2012-09-19,  发布年份 2012
PDF
【 摘 要 】

Background

Osedax worms use a proliferative root system to extract nutrients from the bones of sunken vertebrate carcasses. The roots contain bacterial endosymbionts that contribute to the nutrition of these mouthless and gutless worms. The worms acquire these essential endosymbionts locally from the environment in which their larvae settle. Here we report on the temporal dynamics of endosymbiont diversity hosted by nine Osedax species sampled during a three-year investigation of an experimental whale fall at 1820-m depth in the Monterey Bay, California. The host species were identified by their unique mitochondrial COI haplotypes. The endosymbionts were identified by ribotyping with PCR primers specifically designed to target Oceanospirillales.

Results

Thirty-two endosymbiont ribotypes associated with these worms clustered into two distinct bacterial ribospecies that together comprise a monophyletic group, mostly restricted to deep waters (>1000 m). Statistical analyses confirmed significant changes in the relative abundances of host species and the two dominant endosymbiont ribospecies during the three-year sampling period. Bone type (whale vs. cow) also had a significant effect on host species, but not on the two dominant symbiont ribospecies. No statistically significant association existed between the host species and endosymbiont ribospecies.

Conclusions

Standard PCR and direct sequencing proved to be an efficient method for ribotyping the numerically dominant endosymbiont strains infecting a large sample of host individuals; however, this method did not adequately represent the frequency of mixed infections, which appears to be the rule rather than an exception for Osedax individuals. Through cloning and the use of experimental dilution series, we determined that minority ribotypes constituting less than 30% of a mixture would not likely be detected, leading to underestimates of the frequency of multiple infections in host individuals.

【 授权许可】

   
2012 Salathé and Vrijenhoek; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150324154046743.pdf 1589KB PDF download
Figure 5. 95KB Image download
Figure 4. 101KB Image download
Figure 3. 91KB Image download
Figure 2. 85KB Image download
Figure 1. 170KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】
  • [1]Koslow T: The Silent Deep. The University of Chicago Press, Chicago; 2007.
  • [2]Dubilier N, Bergin C, Lott C: Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 2008, 6:725-740.
  • [3]Vrijenhoek RC: Genetics and evolution of deep-sea chemosynthetic bacteria and their invertebrate hosts. The Vent and Seep Biota, Topics in Geobiology 2010, 33:201015-201050.
  • [4]Bright M, Bulgheresi S: A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 2010, 8:218-230.
  • [5]Katz S, Klepal W, Bright M: The Osedax trophosome: organization and ultrastructure. Biol Bull 2011, 220:128-139.
  • [6]Halanych KM, Feldman RA, Vrijenhoek RC: Molecular evidence that Sclerolinum brattstromi is closely related to vestimentiferans, not frenulate pogonophorans (Siboglinidae, Annelida). Biol Bull 2001, 201:65-75.
  • [7]Rouse GW: A cladistic analysis of Siboglinidae Caullery, 1914 (Polychaeta, Annelida): formerly the phyla Pogonophora and Vestimentifera. Zoological Journal of the Linnean Society 2001, 132:55-80.
  • [8]Rouse GW, Goffredi SK, Vrijenhoek RC: Osedax: Bone-eating marine worms with dwarf males. Science 2004, 305:668-671.
  • [9]McMullin E, Hourdez S, Schaeffer SW, Fisher CR: Phylogeny and biogeography of deep sea vestimentiferans and their bacterial symbionts. Symbiosis 2003, 34:1-41.
  • [10]Thornhill DJ, Wiley AA, Campbell AL, Bartol FF, Teske A, Halanych KM: Endosymbionts of Siboglinum fiordicum and the phylogeny of bacterial endosymbionts in Siboglinidae (Annelida). Biol Bull 2008, 214:135-144.
  • [11]Goffredi SK, Orphan VJ, Rouse GW, Jahnke L, Embaye T, Turk K, Lee R, Vrijenhoek RC: Evolutionary innovation: a bone-eating marine symbiosis. Environ Microbiol 2005, 7:1369-1378.
  • [12]Fujikura K, Fujiwara Y, Kawato M: A new species of Osedax (Annelida: Siboglinidae) associated with whale carcasses off Kyushu, Japan. Zoolog Sci 2006, 23:733-740.
  • [13]Glover AG, Käilström B, Smith CR, Dahlgren TG: World-wide whale worms? A new species of Osedax from the shallow north Atlantic. Proceedings of the Royal Society of London: Biological Sciences 2005, 272:2587-2592.
  • [14]Rouse GW, Worsaae K, Johnson SB, Jones WJ, Vrijenhoek RC: Acquisition of dwarf male ‘harems’ by recently settled females of Osedax roseus n. sp. (Siboglinidae; Annelida). Biol Bull 2008, 214:67-82.
  • [15]Vrijenhoek RC, Johnson SB, Rouse GW: A remarkable diversity of bone-eating worms (Osedax; Siboglinidae; Annelida). BMC Biol 2009, 7:74. 13 pages BioMed Central Full Text
  • [16]Goffredi SK, Johnson SB, Vrijenhoek RC: Genetic diversity and potential function of microbial symbionts associated with newly discovered species of Osedax polychaete worms. Appl Environ Microbiol 2007, 73:2314-2323.
  • [17]Miyazaki M, Nogi Y, Fujiwara Y, Kawato M, Kubokawa K, Horikoshi K: Neptunomonas japonica sp. nov., an Osedax japonicus symbiont-like bacterium isolated from sediment adjacent to sperm whale carcasses off Kagoshima, Japan. Int J Syst Evol Microbiol 2008, 58:866-871.
  • [18]Verna C, Ramette A, Wiklund H, Dahlgren T, Glover A, Gaill F, Dubilier N: High symbiont diversity in the bone-eating worm Osedax mucofloris from shallow whale-falls in the North Atlantic. Environ Microbiol 2010, 12:2355-2370.
  • [19]Katz S, Klepal W, Bright M: The skin of Osedax (Siboglinidae, Annelida): An ultrastructural investigation of its epidermis. J Morphol 2010, 271:1272-1280.
  • [20]Rouse GW, Wilson NG, Goffredi SK, Johnson SB, Smart T, Widmer C, Young CM, Vrijenhoek RC: Spawning and development in Osedax boneworms (Siboglinidae, Annelida). Mar Biol 2009, 156:395-405.
  • [21]Nussbaumer AD, Fisher CR, Bright M: Horizontal endosymbiont transmission in hydrothermal vent tubeworms. Nature 2006, 441:345-348.
  • [22]Rouse GW, Goffredi SK, Johnson SB, Vrijenhoek RC: Not whale-fall specialists, Osedax worms also consume fishbones. Biol Lett 2011, 7:736-739.
  • [23]Stackebrandt E, Goebel BM: Taxonomic note: a place for DNA:DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 1994, 44:846-849.
  • [24]Day MD, Beck D, Foster JA: Microbial Communities as Experimental Units. Bioscience 2011, 61:398-406.
  • [25]Braby CE, Rouse GW, Johnson SB, Jones WJ, Vrijenhoek RC: Bathymetric and temporal variation among Osedax boneworms and associated megafauna on whale-falls in Monterey Bay, California. Deep-Sea Res I Oceanogr Res Pap 2007, 54:1773-1791.
  • [26]Lundsten L, Fraisier K, Schlining KL, Johnson SB, Kuhnz LA, Harvey JB, Clague G, Vrijenhoek RC: Time-series analysis of six whale-fall communities in Monterey Canyon, California, USA. Deep-Sea Res I Oceanogr Res Pap 2010, 57:1573-1584.
  • [27]Jones WJ, Johnson SB, Rouse GW, Vrijenhoek RC: Marine worms (genus Osedax) colonize cow bones. Proceedings of the Royal Society of London: Biological Sciences 2008, 275:387-391.
  • [28]Larkin M, Blackshields G, Brown N, Chenna R, McGettigan P, McWilliam H, Valentin F, Wallace I, Wilm A, Lopez R, et al.: Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948. [ http://www.clustal.org/clustal2/ webcite]
  • [29]Maddison WP, Maddison DR: MacClade (Ver. 4.0): Computer Program for Phylogenetic Analysis. 4.08 edn. Sinauer Associates, Inc, Sunderland, MA; 2005. [ http://macclade.org webcite]
  • [30]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 2011, 28:2731-2739. [ http://www.megasoftware.net/ webcite]
  • [31]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704. [ http://www.lirmm.fr/w3ifa/MAAS/ webcite]
  • [32]Posada D: jModelTest: Phylogenetic Model Averaging. Mol Biol Evol 2008, 25:1253-1256. [ http://darwin.uvigo.es/software/jmodeltest.html webcite]
  • [33]Huelsenbeck JP, Ronquist F: MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755. [ http://bioinformatics.oupjournals.org/cgi/content/abstract/17/8/754 webcite]
  • [34]Ronquist F, Huelsenbeck JP: MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574. [ http://mrbayes.sourceforge.net/ webcite]
  • [35]Rambaut A, Drummond A: Tracer 1.3. University of Oxford, Rambaut Research Group, Oxford, UK; 2003. [ http://evolve.zoo.ox.ac.uk/ webcite]
  • [36]Morariu V, Srinivasan BV, Raykar VC, Duraiswami R, Davis LS: Automatic online tuning for fast Gaussian summation. Advances in Neural Information Processing Systems (NIPS) 2008. [ http://www.umiacs.umd.edu/~morariu/figtree/ webcite]
  • [37]Clement M, Posada D, Crandall KA: TCS: a computer program to estimate gene genealogies. Mol Ecol 2000, 4:331-346.
  • [38]JMP: ver 7. SAS Institute, Inc, Cary, NC, USA; 2007.
  • [39]Nelson K, Fisher C: Absence of cospeciation in deep-sea vestimentiferan tube worms and their bacterial endosymbionts. Symbiosis 2000, 28:1-15.
  • [40]Agresti A: Categorical Data Analysis. John Wiley, New York; 1990.
  • [41]Vrijenhoek RC, Johnson S, Rouse GW: Bone-eating Osedax females and their “harems” of dwarf males are recruited from a common larval pool. Mol Ecol 2008, 17:4535-4544.
  • [42]Cohan FM: Bacterial species and speciation. Syst Zool 2001, 50:513-524.
  • [43]Stackebrandt E, Frederiksen W, Garrity GM, Grimont PAD, Kämpfer P, Maiden MCJ, Nesme X, Rosselló-Mora R, Swings J, Trüper HG, et al.: Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 2002, 52:1043-1047.
  • [44]Goffredi S, Wilpiszeski R, Lee R, Orphan V: Temporal evolution of methane cycling and phylogenetic diversity of archaea in sediments from a deep-sea whale-fall in Monterey Canyon, California. ISME J 2008, 2:204-220.
  • [45]Stewart FJ, Cavanaugh CM: Pyrosequencing analysis of endosymbiont population structure: co-occurrence of divergent symbiont lineages in a single vesicomyid host clam. Environ Microbiol 2009, 11:2136-2147.
  文献评价指标  
  下载次数:21次 浏览次数:2次