Abstract
The pool of mobile genetic elements (MGE) in microbial communities consists of viruses, plasmids, and associated elements (insertion sequences, transposons, and integrons) that are either self-transmissible or use mobile plasmids and viruses as vehicles for their dissemination. This mobilome facilitates the horizontal transfer of genes that promote the evolution and adaptation of microbial communities. Efforts to characterize MGEs from microbial populations resident in a variety of ecological habitats have revealed a surprisingly novel and seemingly untapped biodiversity. To better understand the impact of horizontal gene transfer (HGT), as well as the agents that promote HGT in marine ecosystems and to determine whether or not environmental parameters can effect the composition and structure of the mobilome in marine microbial communities, information on the distribution, diversity, and ecological traits of the marine mobilome is presented. In this chapter we discuss recent insights gained from different methodological approaches used to characterize the biodiversity and ecology of MGE in marine environments and their contributions to HGT. In addition, we present case studies that highlight specific HGT examples in coastal, open-ocean, and deep-sea marine ecosystems.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Ochman, H., Lawrence, J. G., Groisman, E. A. (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299–304.
Mazel, J., Davies, J. (1999) Antibiotic resistance in microbes. Cell Mol Life Sci 56, 742–54.
Tschape, H. (1994) The spread of plasmids as a function of bacterial adaptability. FEMS Microbiol Ecol 15, 23–32.
Staley, J. T., Konopka, A. (1985) Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Ann Rev Microbiol 39, 321–46.
Smalla, K., Sobecky, P. A. (2002) The prevalence and diversity of mobile genetic elements in bacterial communities of different environmental habitats: insights gained from different methodological approaches. FEMS Microbiol Ecol 42, 165–75.
Maniatis, T., Fritsch, E. F., Sambrook, J. (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
Birnboim, H. C., Doly, J. (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids 7, 1513–23.
Kieser, T. (1984) Factors affecting the isolation of ccc DNA from Streptomyces lividans and Escherichia coli. Plasmid 12, 19–36.
Eckhardt, T. (1978) A rapid method for the identification of plasmid deoxyribonucleic acid in bacteria. Plasmid 1, 584–8.
Giovannoni, S., Stingl, U. (2007) The importance of culturing bacterioplankton in the ‘omics’ age. Nat Rev Microbiol 5, 820–6.
Sobecky, P. A., Mincer, T. J., Chang, M. C., Helinski, D. R. (1997) Plasmids isolated from marine sediment microbial communities contain replication and incompatibility regions unrelated to those of known plasmid groups. Appl Environ Microbiol 63, 888–95.
Sobecky, P. A., Mincer, T. J., Chang, M. C., Toukdarian, A., Helinski, D. R. (1998) Isolation of broad-host-range replicons from marine sediment bacteria. Appl Environ Microbiol 64, 2822–30.
Baya, A. M., Brayton, P. R., Brown, V. L., Grimes, D. J., Russek-Cohen, E., Colwell, R. R. (1986) Coincident plasmids and antimicrobial resistance in marine bacteria isolated from polluted and unpolluted Atlantic Ocean samples. Appl Environ Microbiol 51, 1285–92.
Leahy, J. G., Somerville, C. C., Cunningham, K. A., Adamantiades, G. A., Byrd, J. J., Colwell, R. R. (1990) Hydrocarbon mineralization in sediments and plasmid incidence in sediment bacteria from the Campeche Bank. Appl Environ Microbiol 56, 1565–70.
Belliveau, B. H., Starodub, M. E., Trevors, J. T. (1991) Occurrence of antibiotic and metal resistance and plasmids in Bacillus strains isolated from marine sediment. Can J Microbiol 37, 513–20.
Sobecky, P. A. (2002) Approaches to investigating the ecology of plasmids in marine bacterial communities. Plasmid 48, 213–21.
Lopez-Amoros, R., Vives-Rego, J., Garcia-Lara, J. (1997) Exogenous isolation of Hg-r plasmids from coastal Mediterranean waters and their effect on growth and survival of Escherichia coli in sea water. Microbios 92, 3633–40.
Dahlberg, C., Linberg, C., Torsvik, V. L., Hermansson, M. (1997) Conjugative plasmids isolated from bacteria in marine environments show various degrees of homology to each other and are not closely related to well-characterized plasmids. Appl Environ Microbiol 63, 4692–7.
Weinbauer, M. G. (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28, 127–81.
Fuhrman, J. A. (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399, 541–8.
Suttle, C. A. (2007) Marine viruses – major players in the global ecosystem. Nat Rev Microbiol 5, 801–12.
Wen, K., Ortmann, A. C., Suttle, C. A. (2004) Accurate estimation of viral abundance by epifluorescence microscopy. Appl Environ Microbiol 70, 3862–7.
Wichels, A., Gerdts, G., Schutt, C. (2002) Pseudoalteromonas spp. phages, a significant group of marine bacteriophages in the North Sea. Aquatic Microb Ecol 27, 233–9.
Cook, M. A., Osborn, A. M., Bettandorff, J., Sobecky, P. A. (2001) Endogenous isolation of replicon probes for assessing plasmid ecology of marine sediment microbial communities. Microbiology 147, 2089–101.
Cochran, P. K., Paul, J. H. (1998) Seasonal abundance of lysogenic bacteria in a subtropical estuary. Appl Environ Microbiol 64, 2308–12.
Angly, F. E., Felts, B., Breitbart, M., Salamon, P., Edwards, R. A., Carlson, C., Chan, A. M., Haynes, M., Kelley, S., Liu, H., Mahaffy, J. M., Mueller, J. E., Nulton, J., Olson, R., Parsons, R., Rayhawk, S., Suttle, C. A., Rohwer, F. (2006) The marine viromes of four oceanic regions. Plos Biol 4, 2121–31.
Jones, B. V., Marchesi, J. R. (2007) Transposon-aided capture (TRACA) of plasmids resident in the human gut mobile metagenome. Nat Methods 4, 55–61.
Chen, C. Y., Wu, K. M., Chang, C., Chang, C. H., Tsai, H. C., Liao, T. L., Liu, Y. M., Chen, H. J., Shen, A. B., Li, J. C., Su, T. L., Shao, C. P., Lee, C. T., Hor, L. I., Tsai, S. F. (2003) Comparative genome analysis of Vibrio vulnificus, a marine pathogen. Genome Res 13, 2577–87.
Klotz, M. G., Arp, D. J., Chain, P. S., El-Sheikh, A. F., Hauser, L. J., Hommes, N. G., Larimer, F. W., Malfatti, S. A., Norton, J. M., Poret-Peterson, A. T., Vergez, L. M., Ward, B. B. (2006) Complete genome sequence of the marine, chemolithoautotrophic, ammonia-oxidizing bacterium Nitrosococcus oceani ATCC 19707. Appl Environ Microbiol 72, 6299–315.
Swingley, W. D., Sadekar, S., Mastrian, S. D., Matthies, H. J., Hao, J., Ramos, H., Acharya, C. R., Conrad, A. L., Taylor, H. L., Dejesa, L. C., Shah, M. K., O’huallachain, M. E., Lince, M. T., Blankenship, R. E., Beatty, J. T., Touchman, J. W. (2007) The complete genome sequence of Roseobacter denitrificans reveals a mixotrophic rather than photosynthetic metabolism. J Bacteriol 189, 683–90.
Zhou, F., Olman, V., Xu, Y. (2008) Insertion sequences show diverse recent activities in Cyanobacteria and Archaea. BMC Genomics 9, 36–47.
Breitbart, M., Salamon, P., Andresen, B., Mahaffy, J. M., Segall, A. M., Mead, D., Azam, F., Rohwer, F. (2002) Genomic analysis of uncultured marine viral communities. Proc Natl Acad Sci U S A 99, 14250–5.
Culley, A. I., Lang, A. S., Suttle, C. A. (2006) Metagenomic analysis of coastal RNA virus communities. Science 312, 1795–8.
Villemur, R. (1990) The DNA sequence and structural organization of the GC2 plasmid from the red alga Gracilaria chilensis. Plant Mol Biol 15, 237–43.
Moon, D. A., Goff, L. J. (1997) Molecular characterization of two large DNA plasmids in the red alga Porphyra pulchra. Curr Genetics 32, 132–8.
Casse, N., Bui, Q. T., Nicolas, V., Renault, S., Bigot, Y., Laulier, M. (2006) Species sympatry and horizontal transfer of Mariner transposons in marine crustacean genomes. Mol Phylogenet Evol 40, 609–19.
Bult, C. J., White, O., lsen, G. J., Zhou, L., Fleischmann, R. D., Sutton, G. G., Blake, J. A., Fitzgerald, L. M., Clayton, R. A., Gocayne, J. D., Kerlavage, A. R., Dougherty, B. A., Tomb, J., Adams, M. D., Reich, C. I., Overbeek, R., Kirkness, E. F., Weinstock, K. G., Merrick, J. M., Glodek, A., Scott, J. L., Geoghagen, M, N. S., Weidman, J. F., Fuhrmann, J. L., Nguyen, D., Utterback, T. R., Kelley, J. M., Peterson, J. D., Sadow, P. W., Hanna, M. C., Cotton, M. D., Roberts, K. M., Hurst, M. A., Kaine, B. P., Borodovsky, M., Klenk, H., Fraser, C. M., Smith, H. O., Woese, C. R., Venter, J. C. (1996) Complete genome sequence of the methanogenic Archaeon, Methanococcus jannaschii. Science 273, 1058–73.
Comeau, A. M., Chan, A. M., Suttle, C. A. (2006) Genetic richness of vibriophages isolated in a coastal environment. Environ Microbiol 8, 1164–76.
Comeau, A. M., Buenaventura, E., Suttle, C. A. (2005) A persistent, productive, and seasonally dynamic vibriophage population within Pacific oysters (Crassostrea gigas). Appl Environ Microbiol 71, 5324–31.
Shivu, M. M., Rajeeva, B. C., Girisha, S. K., Karunasagar, I., Krohne, G., Karunasagar, I. (2007) Molecular characterization of Vibrio harveyi bacteriophages isolated from aquaculture environments along the coast of India. Environ Microbiol 9, 322–31.
Beeson, K. E., Erdner, D. L., Bagwell, C. E., Lovell, C. R., Sobecky, P. A. (2002) Differentiation of plasmids in marine diazotroph assemblages determined by randomly amplified polymorphic DNA analysis. Microbiology 148, 179–89.
Lindell, D., Sullivan, M. B., Johnson, Z. I., Tolonen, A. C., Rohwer, F., Chisholm, S. (2004) Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc NatlAcad Sci U S A 101, 11013–8.
Zhong, Z., Toukdarian, A., Helinski, D., Knauf, V., Sykes, S., Wilkinson, J. E., O’bryne, C., Shea, T., Deloughery, C., Caspi, R. (2001) Sequence analysis of a 101-kilobase plasmid required for agar degradation by a Microscilla isolate. Appl Environ Microbiol 67, 5771–9.
Zhong, Z., Caspi, R., Mincer, T., Helinski, D., Knauf, V., Boardman, K., Wilkinson, J. E., Shea, T., Deloughery, C., Toukdarian, A. (2002) A 50-kb plasmid rich in mobile gene sequences isolated from a marine micrococcus. Plasmid 47, 1–9.
Short, C. M., Suttle, C. A. (2005) Nearly identical bacteriophage structural gene sequences are widely distributed in both marine and freshwater environments. Appl Environ Microbiol 71, 480–6.
Waldor, M. K., Tschäpe, H., Mekalanos J. J. (1996) A new type of conjugative transposon encodes resistance to sulfamethoxazole, trimethoprim, and streptomycin in Vibrio cholerae O139. J Bacteriol 178, 4157–65.
Ahmed, A. M., Shinoda, S., Shimamoto, T. (2005) A variant type of Vibrio cholerae SXT element in a multidrug-resistant strain of Vibrio fluvialis. FEMS Microbiol Lett 242, 241–7.
Geslin, C., Gaillard, M., Flament, D., Rouault, K., Romancer, M. L., Prieur, D., Erauso, G. (2007) Analysis of the first genome of a hyperthermophilic marine virus-like particle, PAV1, isolated from Pyrococcus abyssi. J Bacteriol 189, 4510–9.
Zhong, Z., Caspi, R., Helinski, D., Knauf, V., Sykes, S., O’ Byrne, C., Shea, T. P., Wilkinson, J. E., De Loughery, C., Toukdarian, A. (2003) Nucleotide sequence based characterizations of two cryptic plasmids from the marine bacterium Ruegeria isolate PR1b. Plasmid 49, 233–52.
Purdy, A., Rohwer, F., Edwards, R., Azam, F., Bartlett, D. H. (2005) A glimpse into the expanded genome content of Vibrio cholerae through identification of genes present in environmental strains. J Bacteriol 187, 2992–3001.
Zhang, R., Wang, Y., Leung, P. C., Gu, J. D. (2007) pVC, a small cryptic plasmid from the environmental isolate of Vibrio cholerae MP-1. J Microbiol 45, 193–8.
Dunn, A. K., Martin, M. O., Stabb, E. V. (2005) Characterizatioon of pES213, a small mobilizable plasmid from Vibrio fischeri. Plasmid 54, 114–34.
Hazen, T. H., Wu, D., Eisen, J. A., Sobecky, P. A. (2007) Sequence characterization and comparative analysis of three plasmids isolated from environmental Vibrio spp. Appl Environ Microbiol 73, 7703–10.
Mcdaniel, L., Paul, J. H. (2005) Effect of nutrient addition and environmental factors on prophage induction in natural populations of marine Synechococcus species. Appl Environ Microbiol 71, 842–50.
Arrigo, K. R. (2005) Marine microorganisms and global nutrient cycles. Nature 437, 349–55.
Waldor, M. K., Mekalanos, J. J. (1996) Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272, 1910–4.
Nasu, H., Iida, T., Sugahara, T., Yamaichi, Y., Park, K. S., Yokoyama, K., Makino, K., Shinagawa, H., Honda, T. (2000) A filamentous phage associated with recent pandemic Vibrio parahaemolyticus O3: K6 strains. J Clin Microbiol 38, 2156–61.
Miller, E. S., Heidelberg, J. F., Eisen, J. A., Nelson, W. C., Durkin, A. S., Ciecko, A., Feldblyum, T. V., White, O., Paulsen, I. T., Nierman, W. C., Lee, J., Szczypinski, B., Fraser, C. M. (2003) Complete genome sequence of the broad-host-range vibriophage KVP40: Comparative genomics of a T4-rel- ated bacteriophage. J Bacteriol 185, 5220–33.
Comeau, A. M., Suttle, C. A. (2007) Distribution, genetic richness, and phage sensitivity of Vibrio spp. from coastal British Columbia. Environ Microbiol 9, 1790–800.
Nishibuchi, M., Kaper, J. B. (1995) Thermostable direct hemolysin gene of Vibrio parahaemolyticus: a virulence gene acquired by a marine bacterium. Infec Immun 63, 2093–9.
Vadivelu, J., Puthucheary, S. D., Mitin, A., Wan, C. Y., Van Melle, B., Puthucheary, J. A. (1996) Hemolysis and plasmid profiles of Vibrio parahaemolyticus. Southeast Asian J Trop Med Pub Health 27, 126–31.
Di Lorenzo, M., Stork, M., Tolmasky, M. E., Actis, L. A., Farrell, D., Welch, T. J., Crosa, L. M., Wertheimer, A. M., Chen, Q., Salinas, P., Waldbeser, L., Crosa, J. H. (2003) Complete sequence of virulence plasmid pJM1 from the marine fish pathogen Vibrio anguillarum strain 775. J Bacteriol 185, 5822–30.
Wu, H., Ma, Y., Zhang, Y., Zhang, H. (2004) Complete sequence of virulence plasmid pEIB1 from the marine fish pathogen Vibrio anguillarum strain MVM425 and location of its replication region. J Appl Microbiol 97, 1021–8.
Lee, C., Amaro, C., Sanjuán, E., Hor, L. (2005) Identification of DNA sequences specific for Vibrio vulnificus Biotype 2 strains by suppression subtractive hybridization. Appl Environ Microbiol 71, 5593–7.
Lee, C. T., Amaro, C., Wu, K. M., Valiente, E., Change, Y. F., Tsai, S. F., Chang, C. H., Hor, L. I. (2008) A common virulence plasmid in biotype 2 Vibrio vulnificus and its dissemination aided by a conjugal plasmid. J Bacteriol 190, 1638–48.
Culley, A. I., Lang, A. S., Suttle, C. A. (2003) High diversity of unknown picorna-like viruses in the sea. Nature 424, 1054–7.
Culley, A. I., Lang, A. S., Suttle, C. A. (2006) Metagenomic analysis of coastal RNA virus communities. Science 312, 1795–8.
Koenig, J. E., Boucher, Y., Charlebois, R. L., Nesbo, C., Zhaxybayeva, O., Bapteste, E., Spencer, M., Joss, M. J., Stokes, H. W., Doolittle, W. F. (2008) Integron-associated gene cassettes in Halifax Harbour: assessment of a mobile gene pool in marine sediments. Environ Microbiol doi:10:1111/j.1462-2920.20007.01524.x.
Nesbo, C. L., Boucher, Y., Dlutek, M., Doolittle, W. F. (2005) Lateral gene transfer and phylogenetic assignment of environmental fosmid clones. Environ Microbiol 7, 2011–26.
Biers, E. J., Wang, K., Pennington, C., Belas, R., Chen, F., Moran, M. A. (2008) Occurrence and expression of gene transfer agent (GTA) genes in marine bacterioplankton. Appl Environ Microbiol doi:10.1128/AEM.02129-07.
Lang, A. S., Beatty, J. T. (2007) Importance of widespread gene transfer agent genes in alpha-proteobacteria. Trends Microbiol 15, 54–62.
Veldhuis, M. J. W., Kraay, G. W., Vanbleijswijk, J. D., L., Baars, M. A. (1997) Seasonal and spatial variability in phytoplankton biomass, productivity, and growth in the northwestern Indian Ocean: the southwest and northeast monsoon, 1992–1993. Deep-Sea Res Part I-Oceanographic Res Papers 44, 425–49.
Zeidner, G., Bielawski, J. P., Shmoish, M., Scanlan, D. J., Sabehi, G., Beja, O. (2005) Potential photosynthesis gene recombination between Prochlorococcus and Synechococcus via viral intermediates. Environ Microbiol 7, 1505–13.
Millard, A., Clokie, M. R. J., Shub, D. A., Mann, N. H. (2004) Genetic organization of the psbAD region in phages infecting marine Synechococcus strains. Proc Natl Acad Sci U S A 101, 11007–12.
Mann, N. H., Cook, A., Millard, A., Bailey, S., Clokie, M. (2003) Marine ecosystems: Bacterial photosynthesis genes in a virus. Nature 424, 741.
He, Q. F., Dolganov, N., Bjorkman, O., Grossman, A. R. (2001) The high light-inducible polypeptides in Synechocystis PCC6803 – Expression and function in high light. J Biol Chem 276, 306–14.
Frigaard, N. U., Martinez, A., Mincer, T. J., Delong, E. F. (2006) Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea. Nature 439, 847–50.
Mccarren, J., Delong, E. F. (2007) Proteorhodopsin photosystem gene clusters exhibit co-evolutionary trends and shared ancestry among diverse marine microbial phyla. Environ Microbiol 9, 846–58.
Nelson, K. E., Clayton, R. A., Gill, S. R., Gwinn, M. L., Dodson, R. J., Haft, D. H., Hickey, E. K., Peterson, L. D., Nelson, W. C., Ketchum, K. A., Mcdonald, L., Utterback, T. R., Malek, J. A., Linher, K. D., Garrett, M. M., Stewart, A. M., Cotton, M. D., Pratt, M. S., Phillips, C. A., Richardson, D., Heidelberg, J., Sutton, G. G., Fleischmann, R. D., Eisen, J. A., White, O., Salzberg, S. L., Smith, H. O., Venter, J. C., Fraser, C. M. (1999) Evidence for lateral gene transfer between Archaea and Bacteria from the genome sequence of Thermotoga maritima. Nature 399, 323–9.
Jorgensen, B. B., Boetius, A. (2007) Feast and famine-microbial life in the deep-sea bed. Nat Microbiol 5, 770–81.
Munoz, E., Villadas, P. J., Toro, N. (2001) Ectopic transposition of a group II intron in natural bacterial populations. Mol Microbiol 41, 645–52.
Podar, M., Mullineaux, L., Huang, H. R., Perlman, P. S., Sogin, M. L. (2002) Bacterial group II introns in a deep-sea hydrothermal vent environment. Appl Environ Microbiol 68, 6392–8.
Moussard, H., Moreira, D., Cambon-Bonavita, M. A., Lopez-Garcia, P., Jeanthon, C. (2006) Uncultured Archaea in a hydrothermal microbial assemblage: phylogenetic diversity and characterization of a genome fragment from a euryarchaeote. FEMS Microbiol Ecol 57, 452–69.
Lopez-Garcia, P., Brochier, C., Moreira, D., Rodriguez-Valera, F. (2004) Comparative analysis of a genome fragment of an uncultivated mesopelagic crenarchaeote reveals multiple horizontal gene transfers. Environ Microbiol 6, 19–34.
Okamoto, T., Maruyama, A., Imura, S., Takeyama, H., Naganuma, T. (2004) Comparative phylogenetic analyses of Halomonas variabilis and related organisms based on 16S rRNA, gyrB, and ectBC gene sequences. Syst Appl Microbiol 27, 323–33.
Johnson, E. F., Mukhopadhyay, B. (2005) A new type of sulfite reductase, a novel coenzyme F-420-dependent enzyme, from the methanarchaeon Methanocaldococcus jannaschii. J Biol Chem 280, 38776–86.
Tamegai, H., Kato, C., Horikoshi, K. (2004) Lateral gene transfer in the deep sea of Mariana trench: identification of nar gene cluster encoding membrane-bound nitrate reductase from Pseudomonas sp. strain MT-1. DNA Sequence 15, 338–43.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2009 Humana Press, a part of Springer Science+Business Media, LLC
About this protocol
Cite this protocol
Sobecky, P.A., Hazen, T.H. (2009). Horizontal Gene Transfer and Mobile Genetic Elements in Marine Systems. In: Gogarten, M.B., Gogarten, J.P., Olendzenski, L.C. (eds) Horizontal Gene Transfer. Methods in Molecular Biology, vol 532. Humana Press. https://doi.org/10.1007/978-1-60327-853-9_25
Download citation
DOI: https://doi.org/10.1007/978-1-60327-853-9_25
Publisher Name: Humana Press
Print ISBN: 978-1-60327-852-2
Online ISBN: 978-1-60327-853-9
eBook Packages: Springer Protocols