全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2012 

Antibiotic-Induced Change of Bacterial Communities Associated with the Copepod Nitocra spinipes

DOI: 10.1371/journal.pone.0033107

Full-Text   Cite this paper   Add to My Lib

Abstract:

Environmental pressures, such as physical factors, diet and contaminants may affect interactions between microbial symbionts and their multicellular hosts. Despite obvious relevance, effects of antimicrobial contaminants on host-symbiont relations in non-target aquatic organisms are largely unknown. We show that exposure to antibiotics had negative effects on survival and juvenile development of the copepod Nitocra spinipes and caused significant alterations in copepod-associated bacterial communities. The significant positive correlations between indices of copepod development and bacterial diversity indicate that disruption of the microflora was likely to be an important factor behind retarded juvenile development in the experimental animals. Moreover, as evidenced by ribotype distribution in the bacterial clone libraries, the exposure to antibiotics caused a shift in dominance from Betaproteobacteria to Cardinium bacteria; the latter have been shown to cause reproductive manipulations in various terrestrial arthropods. Thus, in addition to providing evidence that the antibiotic-induced perturbation of the microbial community associates with reductions in fitness-related traits of the host, this study is the first record of a copepod serving as a host for endosymbiotic Cardinium. Taken together, our results suggest that (1) antimicrobial substances and possibly other stressors can affect micobiome and symbiont-mediated interactions in copepods and other hosts, and (2) Cardinium endosymbionts may occur in other copepods and affect reproduction of their hosts.

References

[1]  Toft C, Andersson SGE (2010) Evolutionary microbial genomics: Insights into bacterial host adaptation. Nat Rev Genet 11: 465–475.
[2]  Sachs JL, Essenberg CJ, Turcotte MM (2011) New paradigms for the evolution of beneficial infections. Trends Ecol Evol 26: 202–209.
[3]  Werren JH (1997) Biology of Wolbachia. Annu Rev Entomol 42: 587–609.
[4]  Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43: 17–37.
[5]  Wilson EO (1992) The diversity of life. New York: W.W. Norton & Company. 424 p.
[6]  Kurtti TJ, Munderloh UG, Andreadis TG, Magnarelli LA, Mather TN (1996) Tick cell culture isolation of an intracellular prokaryote from the tick Ixodes scapularis. J Invert Pathol 67: 318–321.
[7]  Zchori-Fein E, Perlman SJ, Kelly SE, Katzir N, Hunter MS (2004) Characterization of a ‘Bacteroidetes’ symbiont in Encarsia wasps (Hymenoptera: Aphelinidae): proposal of ‘Candidatus Cardinium hertigii’. Int J Syst Evol Microbiol 54: 961–968.
[8]  Zchori-Fein E, Perlman SJ (2004) Distribution of the bacterial symbiont Cardinium in arthropods. Mol Ecol 13: 2009–2016.
[9]  Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH (2008) How many species are infected with Wolbachia? – A statistical analysis of current data. FEMS Microbiol Lett 281: 215–220.
[10]  Hunter MS, Perlman SJ, Kelly SE (2003) A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella. Proc R Soc Lond B Biol Sci 270: 2185–2190.
[11]  Gotoh T, Noda H, Ito S (2007) Cardinium symbionts cause cytoplasmic incompatibility in spider mites. Heredity 98: 13–20.
[12]  Ros VI, Breeuwer JA (2009) The effects of, and interactions between, Cardinium and Wolbachia in the doubly infected spider mite Bryobia sarothamni. Heredity 102: 413–22.
[13]  Parsons TR, Takahashi M, Hargrave B (1977) Biological Oceanographic Processes. 332 p. 2nd edition, Pergamon Press, Oxford.
[14]  St?ttrup J (2000) The elusive copepods: their production and suitability in marine aquaculture. Aquacult Res 31: 703–711.
[15]  Raisuddin S, Kwok KWH, Leung KMY, Schlenk D, Lee JS (2007) The copepod Tigriopus: A promising marine model organism for ecotoxicology and environmental genomics. Aquat Toxicol 83: 161–173.
[16]  Tang K, Dziallas C, Hutalle-Schmelzer K, Grossart HP (2009) Effects of food on bacterial community composition associated with the copepod Acartia tonsa Dana. Biology Letters 5: 549–553.
[17]  Tang KW, Turk V, Grossart HP (2010) Linkage between crustacean zooplankton and aquatic bacteria. Aquat Microb Ecol 61: 261–277.
[18]  Homonnay ZG, Kéki Z, Márialigeti K, Tóth EM (2011) Bacterial communities in the gut of the freshwater copepod Eudiaptomus gracilis. J Basic Microbiol 51: 1–5.
[19]  Kümmerer K (2009) Antibiotics in the aquatic environment – A review – Part I. Chemosphere 75: 417–434.
[20]  Grung M, K?llqvist T, Sakshaug S, Skurtveit S, Thomas KV (2008) Environmental assessment of Norwegian priority pharmaceuticals based on the EMEA guideline. Ecotoxicol Environ Safety 71: 328–340. 20.
[21]  Grung M, K?llqvist T, Sakshaug S, Skurtveit S, Thomas KV (2008) Environmental assessment of Norwegian priority pharmaceuticals based on the EMEA guideline. Ecotoxicol Environ Safety 71: 328–340. 20.Lang, K., 1948. Monographie der Harpacticiden. Vol. II. Ohlsson, Lund, Sweden, 1682 p.
[22]  Halling-Sorensen B, Holten Lutzhoft HC, Andersen HR, Ingerslev F (2000) Environmental risk assessment of antibiotics; comparison of mecillinam, trimethoprim and ciprofloxacin. J Antimicrob Therapy 46: 53–58.
[23]  Robinson AA, lden JB, Lydy MJ (2005) Toxicity of fluoroquinolone antibiotics to aquatic organisms. Environ Toxicol Chem 24: 423–430.
[24]  Straughan DJ, Lehman N (2000) Genetic differentiation among Oregon lake populations of the Daphnia pulex species complex. J Heredity 91: 8–17.
[25]  Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173: 697–703.
[26]  Muyzer G, Teske A, Wirsen CO, Jannasch HW (1995) Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 164: 165–172.
[27]  Altschul SF, Madden TL, Schffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25: 3389–3402.
[28]  Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA-DNA reassociation and 16s rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44: 846–849.
[29]  Hagstr?m A, Pommier T, Rohwer F, Simu K, Stolte W, et al. (2002) Use of 16S ribosomal DNA for delineation of marine bacterioplankton species. Appl Environ Microbiol 68: 3628–3633.
[30]  Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 1–19.
[31]  Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17: 368–376.
[32]  Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML Online—a web server for fast maximum likelihood-based phylogenetic inference. Nucl Acids Res 33: W557–W559.
[33]  Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5: 150–163.
[34]  Nakamura Y, Kawai S, Yukuhiro F, Ito S, Gotoh T, et al. (2009) Prevalence of Cardinium bacteria in planthoppers and spider mites and taxonomic revision of “Candidatus Cardinium hertigii” based on detection of a new Cardinium group from biting midges. Appl Environ Microbiol 75: 6757–6763.
[35]  Magurran AE (1988) Ecological diversity and its measurement. Princeton, NJ: Princeton University Press. 336 p.
[36]  Wilberforce EM, Boddy L, Griffiths R, Griffith GW (2003) Agricultural management affects communities of culturable root-endophytic fungi in temperate grasslands. Soil Biol Biochem 35: 1143–1154.
[37]  Knuckey RM, Semmens GL, Mayer RJ, Rimmer MA (2005) Development of an optimal microalgal diet for the culture of the calanoid copepod Acartia sinjiensis: Effect of algal species and feed concentration on copepod development. Aquaculture 249: 339–351.
[38]  Ferrari B, Mons R, Vollat B, Fraysse B, Paxéus N, et al. (2004) ERA of six human pharmaceuticals: are the current ERA procedures sufficient for the protection of the aquatic environment? Environ Toxicol Chem 23: 1344–1354.
[39]  Wollenberger L, Halling-S?rensen B, Kusk KO (2000) Acute and chronic toxicity of veterinary antibiotics to Daphnia magna. Chemosphere 40: 723–730.
[40]  Kuhlmann I (1996) The prophylactic use of antibiotics in cell culture. Cytotechnology 19: 95–105.
[41]  Rieper M (1982) Feeding preferences of marine harpacticoid copepods for various species of bacteria. Mar Ecol Prog Ser 7: 303–307.
[42]  Ustach JF (1982) Algae, bacteria and detritus as food for the harpacticoid copepod, Heteropsyllus pseudonunni Coull and Palmer. J Exp Mar Biol Ecol 64: 203–214.
[43]  Giordano R, Weber E, Waite J, Bencivenga N, Krogh PH, et al. (2010) Effect of a high dose of three antibiotics on the reproduction of a parthenogenetic strain of Folsomia candida (Isotomidae: Collembola). Environ Entomol 39: 1170–1177.
[44]  Harris JM (1993) The presence, nature, and role of gut microflora in aquatic invertebrates: A synthesis. Microb Ecol 25: 195–231.
[45]  Jeon S, Bunge J, Leslin C, Stoeck T, Hong S, et al. (2008) Environmental rRNA inventories miss over half of protistan diversity. BMC Microbiol 8: 222.
[46]  Green RH (1974) The association of viral activation with penicillin toxicity in Guinea pigs and hamsters. Yale J Biol Medicine 3: 166–181.
[47]  Haine ER (2008) Symbiont-mediated protection. Proc R Soc Lond B 275: 353–361.
[48]  Ahmed M, Stal LJ, Hasnain S (2010) Association of non-heterocystous cyanobacteria with crop plants. Plant Soil 336: 363–375.
[49]  van der Grinten E, Pikkemaat MG, van den Brandhof EJ, Stroomberg GJ, Kraak MH (2010) Comparing the sensitivity of algal, cyanobacterial and bacterial bioassays to different groups of antibiotics. Chemosphere 80: 1–6.
[50]  Lambo AJ, Patel TR (2006) Isolation and characterization of a biphenyl-utilizing psychrotrophic bacterium, Hydrogenophaga taeniospiralis IA3-A, that cometabolize dichlorobiphenyls and polychlorinated biphenyl congeners in Aroclor 1221. J Basic Microbiol 46: 94–107.
[51]  Geib SM, Jimenez-Gasco Mdel M, Carlson JE, Tien M, Hoover K (2009) Effect of host tree species on cellulase activity and bacterial community composition in the gut of larval Asian longhorned beetle. Environ Entomol 38: 686–699.
[52]  Wüst PK, Horn MA, Drake HL (2011) Clostridiaceae and Enterobacteriaceae as active fermenters in earthworm gut content. ISME J 5: 92–106.
[53]  Russell JA, Moreaua CS, Goldman-Huertas B, Fujiwara M, Lohman DJ, et al. (2009) Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc Natl Acad Sci U S A 106: 21236–21241.
[54]  Rawls JR, Mahowald MA, Goodman AL, Trent CM, Gordon JI (2007) In vivo imaging and genetic analysis link bacterial motility and symbiosis in the zebrafish gut. Proc Natl Acad Sci U S A 104: 7622–7627.
[55]  Provencher LM, Morse GE, Weeks AR, Normark BB (2005) Parthenogenesis in the Aspidiotus nerii Complex (Hemiptera: Diaspididae): A Single Origin of a Worldwide, Polyphagous Lineage Associated with Cardinium Bacteria. Ann Entomol Soc Am 98: 629–635.
[56]  Gusm?o LFM, McKinnon AD (2009) Sex ratios, intersexuality and sex change in copepods. J Plankton Res 31: 1101–1117.
[57]  Thistle D, Eckman JE (1990) What is the sex ratio of harpacticoid copepods in the deep sea? Mar Biol 107: 443–447.
[58]  Hirst AG, Bonnet D, Conway DVP, Ki?rboe T (2010) Does predation control adult sex ratios and longevities in marine pelagic copepods? Limnol Oceanogr 55: 2193–2206.
[59]  Voordouw MJ, Stebbins G, Robinson HE, Perrot-Minnot MJ, Rigaud T, et al. (2008) Genetic variation in the primary sex ratio in populations of the intertidal copepod, Tigriopus californicus, is widespread on Vancouver Island. Evol Ecol Res 10: 1007–1023.
[60]  Morimoto S, Kurtti TJ, Noda H (2006) In vitro cultivation and antibiotic susceptibility of a Cytophaga-like intracellular symbiote isolated from the tick Ixodes scapularis. Curr Microbiol 52: 324–329.
[61]  Falconer SB, Czarny TL, Brown ED (2011) Antibiotics as probes of biological complexity. Nature Chem Biol 415–423.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133