Skip to main content
Log in

Taxonomic and metabolic shifts in the Coorong bacterial metagenome driven by salinity and external inputs

  • Published:
Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

The Coorong estuary lies at the terminus of Australia’s largest river system, the Murray-Darling; both are strongly influenced by human activities; including farming and extensive flow modification. Metagenomic approaches were used to determine the planktonic bacterial community composition and potential metabolic function at two extremes in the Coorong, the river mouth which exhibits marine-like salinity, and the hypersaline upper-reaches of the estuary. Significant shifts in taxa and metabolic function were seen between the two sites. The river mouth exhibited an increase in abundance of Rhodobacteriaceae and Alteromonadaceae; families readily able to adapt to change in nutrient conditions; and the potentially pathogenic families Brucellaceae, Enterobacteriaceae and Vibrionaceae. Metabolisms over-represented include motility and chemotaxis, RNA metabolism and membrane transport, all of which are involved in actively searching for and obtaining nutrients. Also over-represented were metabolisms involved in population succession and stress response. An over-representation of taxa and metabolisms indicative of environmental change is reflective of anthropogenically affected riverine input. In the hypersaline upper reaches of the estuary, the halophilic family Ectothiorhodospiraceae was over-represented, as were the families Flavobacteriaceae, Cytophagaceae and Nocardioidaceae, members of which are able to survive over a wide salinity range. Metabolisms over-represented here were reflective of increased bacterial growth, characteristic of hypersaline environments, and included DNA metabolism, nucleotide and nucleoside synthesis and cell cycle. Coorong metagenomes clustered taxonomically and metabolically with other planktonic metagenomes, but remained an outlier of this group with only 71% and 84% similarity, respectively. This indicates that the Coorong exhibits a unique planktonic bacterial community that is influenced by riverine input at the river mouth and salinity in the upper-reaches.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Allers E, Gómez–Consarnau L, Pinhassi J, Gasol J M, Šimek K, Pernthaler J. 2007. Response of Alteromonadaceae and Rhodobacteriaceae to glucose and phosphorus manipulation in marine mesocosms. Environ. Microbiol., 9 (10): 2 417–2 429.

    Article  Google Scholar 

  • Alonso–Sáez L, Arístegui J, Pinhassi J, Gómez–Consarnau L, González J M, Vaqué D, Agustí S, Gasol J M. 2007. Bacterial assemblage structure and carbon metabolism along a productivity gradient in the NE Atlantic Ocean. Aquat. Microb. Ecol., 46 (1): 43–53.

    Article  Google Scholar 

  • Ayub N D, Pettinari M J, Ruiz J A, López N I. 2004. A polyhydroxybutyrate–producing Pseudomonas sp. Isolated from Antarctic environments with high stress resistance. Curr. Microbiol., 49 (3): 170–174.

    Google Scholar 

  • Azam F, Malfatti F. 2007. Microbial structuring of marine ecosystems. Nat. Rev. Microbiol., 5 (10): 782–791.

    Article  Google Scholar 

  • Barillé–Boyer A L, Barillé L, Massé H, Razet D, Héral M. 2003. Correction for particulate organic matter as estimated by loss on ignition in estuarine ecosystems. Estuar. Coast. Shelf Sci., 58 (1): 147–153.

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Statist. Soc. Ser. B., 57 (1): 289–300.

    Google Scholar 

  • Benlloch S, López–López A, Casamayor E O, Øvreås L, Goddard V, Daae F L, Smerdon G, Massana R, Joint I, Thingstad F, Pedrós–Alió C, Rodríguez–Valera F. 2002. Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. Environ. Microbiol., 4 (6): 349–360.

    Article  Google Scholar 

  • Biers E J, Sun S L, Howard E C. 2009. Prokaryotic genomes and diversity in surface ocean waters: Interrogating the Global Ocean Sampling metagenome. Appl. Environ. Microbiol., 75 (7): 2 221–2 229.

    Article  Google Scholar 

  • Blackburn N, Fenchel T, Mitchell J G. 1998. Microscale nutrient patches in planktonic habitats shown by chemotactic bacteria. Science, 282 (5397): 2 254–2 256.

    Article  Google Scholar 

  • Bouvier T C, del Giorgio P A. 2002. Compositional changes in free–living bacterial communities along a salinity gradient in two temperate estuaries. Limnol. Oceanogr., 47 (2): 453–470.

    Article  Google Scholar 

  • Bowman J P, Nichols D S. 2005. Novel members of the family Flavobacteriaceae from Antarctic maritime habitats including Subsaximicrobium wynnwilliamsii gen. nov., sp. nov., Subsaximicrobium saxinquilinus sp. nov., Subsaxibacter broadyi gen. nov., sp. nov., Lacinutrix copepodicola gen. nov., sp. nov., and novel species of the genera Bizionia, Gelidibacter and Gillisia. Int. J. Syst. Evol. Microbiol., 55 (4): 1 471–1 486.

    Article  Google Scholar 

  • Brindefalk B, Ettema T J G, Viklund J, Thollesson M, Andersson S G E. 2011. A phylometagenomic exploration of oceanic Alphaproteobacteria reveals mitochondrial relatives unrelated to the SAR11 clade. PLoS One, 6 (9): e24457.

    Article  Google Scholar 

  • Brussaard C P D. 2004. Optimization of procedures for counting viruses by flow cytometry. Appl. Environ. Microbiol., 70 (3): 1 506–1 513.

    Article  Google Scholar 

  • Bull A T, Stach J E M, Ward A C, Goodfellow M. 2005. Marine actinobacteria: perspectives, challenges, future directions. Antonie van Leeuwenhoek, 87 (1): 65–79.

    Article  Google Scholar 

  • Cabiscol E, Tamarit J, Ros J. 2000. Oxidative stress in bacteria and protein damage by reactive oxygen species. Int. Microbiol., 3 (1): 3–8.

    Google Scholar 

  • Chapelle F H, Lovley D R. 1990. Rates of microbial metabolism in deep coastal plain aquifers. Appl. Environ. Microbiol., 56 (6): 1 865–1 874.

    Google Scholar 

  • Clarke K R, Gorley R N. 2006. PRIMER v6: User Manual/Tutorial. PRIMER–E, Plymouth, UK.

    Google Scholar 

  • Clarke K R. 1993. Non–parametric multivariate analyses of changes in community structure. Austr. J. Ecol., 18 (1): 117–143.

    Article  Google Scholar 

  • Cottrell M T, Waidner L A, Yu L Y, Kirchman D L. 2005. Bacterial diversity of metagenomic and PCR libraries from the Delaware River. Environ. Microbiol., 7 (12): 1 883–1 895.

    Article  Google Scholar 

  • Cugley J, Shukla C, Sarneckis K. 2002. Ambient Water Quality Monitoring of the River Murray 1990–199. Report No.1. Environment Protection Agency South Australia, Adelaide. 103p.

    Google Scholar 

  • DeLong E F, Preston C M, Mincer T, Rich V, Hallam S J, Frigaard N–U, Martinez A, Sullivan M B, Edwards R, Brito B R, Chisholm S W, Karl D M. 2006. Community genomics among stratified microbial assemblages in the ocean’s interior. Science, 311 (5760): 496–503.

    Article  Google Scholar 

  • Dinsdale E A, Pantos O, Smriga S, Edwards R A, Angly F, Wegley L, Hatay M, Hall D, Brown E, Haynes M, Krause L, Sala E, Sandin S A, Thurber R V, Willis B L, Azam F, Knowlton N, Rohwer F. 2008. Microbial ecology of four coral atolls in the Northern Line Islands. PLoS One, 3 (2): e1584.

    Article  Google Scholar 

  • Dobson S J, Colwell R R, McMeekin T A, Franzmann P D. 1993. Direct sequencing of the polymerase chain reactionamplified 16S rRNA gene of Flavobacterium gondwanense sp. nov. and Flavobacterium salegens sp. nov., two new species from a hypersaline Antarctic lake. Int. J. Syst. Bacteriol., 43 (1): 77–83.

    Article  Google Scholar 

  • Edwards R A, Rodriguez–Brito B, Wegley L, Haynes M, Breitbart M, Peterson D M, Saar M O, Alexander S, Alexander E C, Rohwer F. 2006. Using pyrosequencing to shed light on deep mine microbial ecology. BMC Genomics, 7: 57.

    Google Scholar 

  • Esteban J A, Salas M, Blanco L. 1993. Fidelity of ϕ 29 DNA Polymerase. J. Biol. Chem., 268 (4): 2 719–2 726.

    Google Scholar 

  • Fisher W D. 1958. On grouping for maximum homogeneity. J. Am. Statist. Assoc., 53 (284): 789–798.

    Article  Google Scholar 

  • Ford P W. 2007. Biogeochemistry of the Coorong. Review and identification of future research requirements. CSIRO Water for a Healthy Country National Research Flagship. CSIRO, Canberra. 23p.

    Google Scholar 

  • Garrity G M, Bell J A, Lilburn T. 2005. Family III, Brucellaceae breed, Murray and smith 1957, 394AL. In: Brenner D J, Krieg N R, Staley J T, Garrity G M eds. 2nd edn. Bergey’s Manual of Systematic Bacteriology. Springer, New York. p.370–386.

  • Gasol J M, del Giorgio P A. 2000. Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Sci. Mar., 64 (2): 197–224.

    Article  Google Scholar 

  • Geddes M C. 2005. The ecological health of the North and South Lagoons of the Coorong in July 2004. Report Prepared for the Department of Water, Land and Biodiversity Conservation. SARDI Aquatic Sciences Publication Number RD03/0272–2. South Australian Research and Development Institute (Aquatic Sciences), Adelaide, 29pp.

    Google Scholar 

  • Ghai R, Pašić L, Fernández A B, Martin–Cuadrado A B, Mizuno C M, McMahon K D, Papke R T, Stepanauskas R, Rodriguez–Brito B, Rohwer F, Sánchez–Porro C, Ventosa A, Rodríguez–Valera F. 2011. New abundant microbial groups in aquatic hypersaline environments. Sci. Rep., 1: 135.

    Article  Google Scholar 

  • Guixa–Boixareu N, Calderón–Paz J I, Heldal M, Bratbak G, Pedrós–Alió C. 1996. Viral lysis and bacterivory as prokaryotic loss factors along a salinity gradient. Aquat. Microb. Ecol., 11 (3): 215–227.

    Article  Google Scholar 

  • Han S K, Nedashkovskaya O I, Mikhailov V V, Kim S B, Bae K S. 2003. Salinibacterium amurskyense gen. nov., sp. nov., a novel genus of the family Microbacteriaceae from the marine environment. Int. J. Syst. Evol. Microbiol., 53 (6): 2 061–2 066.

    Article  Google Scholar 

  • Henriques I S, Alves A, Tacão M, Almeida A, Cunha Â, Correia A. 2006. Seasonal and spatial variability of free–living bacterial community composition along an estuarine gradient (Ria de Aveiro, Portugal). Estuar. Coast. Shelf Sci., 68 (1–2): 139–148.

    Article  Google Scholar 

  • Herlemann D P, Labrenz M, Jürgens K, Bertilsson S, Waniek J J, Andersson A F. 2011. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J., 5 (10): 1 571–1 579.

    Article  Google Scholar 

  • Hill D, Owens W, Tchounwou P. 2005. Impact of animal waste application on runoffwater quality in field experimental plots. Int. J. Environ. Res. Public Health, 2 (2): 314–321.

    Article  Google Scholar 

  • Imhoff J F, Süling J. 1996. The phylogenetic relationship among Ectothiorhodospiraceae: a reevaluation of their taxonomy on the basis of 16S rDNA analyses. Arch. Microbiol., 165 (2): 106–113.

    Article  Google Scholar 

  • Ivanova E P, Flavier S, Christen R. 2004. Phylogenetic relationships among marine Alteromonas–like Proteobacteria: emended description of the family Alteromonadaceae and proposal of Pseudoalteromonadaceae fam. nov., Colwelliaceae fam. nov., Shewanellaceae fam. nov., Moritellaceae fam. nov., Ferrimonadaceae fam. nov., Idiomarinaceae fam. nov. and Psychromonadaceae fam. nov. Int. J. Syst. Evol. Microbiol., 54 (5): 1 773–1 788.

    Article  Google Scholar 

  • Jeffries T C, Seymour J R, Gilbert J A, Dinsdale E A, Newton K, Leterme S S C, Roudnew B, Smith R J, Seuront L, Mitchell J G. 2011. Substrate type determines metagenomic profiles from diverse chemical habitats. PLoS One, 6 (9): e25173.

    Article  Google Scholar 

  • Jeffries T C, Seymour J R, Newton K, Smith R J, Seuront L, Mitchell J G. 2012. Increases in the abundance of microbial genes encoding halotolerance and photosynthesis along a sediment salinity gradient. Biogeosciences, 9 (2): 815–825.

    Article  Google Scholar 

  • Jolly I D, Williamson D R, Gilfedder M, Walker G R, Morton R, Robinson G, Jones H, Zhang L, Dowling T I, Dyce P, Nathan R J, Nandakumar N, Clarke R, McNeill V. 2001. Historical stream salinity trends and catchment salt balances in the Murray–Darling Basin, Australia. Mar. Freshw. Res., 52 (1): 53–63.

    Article  Google Scholar 

  • Jones K, Betaieb M. 1986. The dispersal of nitrogen–fixing enterobacteriaceae from sewage in the waters and sediments of Morecambe Bay, UK. Colloque International de Bacteriologie Marine. IFREMER, É ditions du CNRS, Brest, France. p.525–531.

    Google Scholar 

  • Kan J J, Suzuki M T, Wang K, Evans S E, Chen F. 2007. High temporal but low spatial heterogeneity of bacterioplankton in the Chesapeake Bay. Appl. Environ. Microbiol., 73 (21): 6 776–6 789.

    Article  Google Scholar 

  • Kingsford R T, Walker K F, Lester R E, Young W J, Fairweather P G, Sammut J, Geddes M C. 2011. A Ramsar wetland in crisis—the Coorong, Lower Lakes and Murray Mouth, Australia. Mar. Freshw. Res., 62 (3): 255–265.

    Article  Google Scholar 

  • Kiørboe T, Jackson G A. 2001. Marine snow, organic solute plumes, and optimal chemosensory behavior of bacteria. Limnol. Oceanogr., 46 (6): 1 309–1 318.

    Article  Google Scholar 

  • Klatt P, Lamas S. 2000. Regulation of protein function by S–glutathiolation in response to oxidative and nitrosative stress. Eur. J. Biochem., 267 (16): 4 928–4 944.

    Article  Google Scholar 

  • Lamontagne S, McEwan K, Webster I, Ford P, Leaney F, Walker G. 2004. Coorong Lower Lakes and Murray Mouth. Knowledge gaps and knowledge needs for delivering better ecological outcomes. CSIRO Water for a Healthy Country Flagship Report Series. CSIRO, Canberra. 38p.

    Google Scholar 

  • Lasken R S, Stockwell T B. 2007. Mechanism of chimera formation during the multiple displacement amplification reaction. BMC Biotechnol., 7: 19.

    Article  Google Scholar 

  • Lee S D, Lee D W, Kim J S. 2008. Nocardioides hwasunensis sp. nov. Int. J. Syst. Evol. Microbiol., 58 (1): 278–281.

    Article  Google Scholar 

  • Lester R E, Fairweather P G. 2009. Modelling future conditions in the degraded semi–arid estuary of Australia's largest river using ecosystem states. Estuar. Coast. Shelf Sci., 85 (1): 1–11.

    Article  Google Scholar 

  • Lozupone C A, Knight R. 2007. Global patterns in bacterial diversity. Proc. Natl. Acad. Sci. USA, 104 (27): 11 436–11 440.

    Article  Google Scholar 

  • Magarvey N A, Keller J M, Bernan V, Dworkin M, Sherman D H. 2004. Isolation and characterization of novel marinederived actinomycete taxa rich in bioactive metabolites. Appl. Environ. Microbiol., 70 (12): 7 520–7 529.

    Article  Google Scholar 

  • Magurran A E. 2004. Measuring Biological Diversity. Blackwell Science Ltd., Oxford. 264p.

    Google Scholar 

  • Marie D, Brussaard C P D, Thyrhaug R, Bratbak G, Vaulot D. 1999a. Enumeration of marine viruses in culture and natural samples by flow cytometry. Appl. Environ. Microbiol., 65 (1): 45–52.

    Google Scholar 

  • Marie D, Partensky F, Vaulot D, Brussaard C. 1999b. Numeration of phytoplankton, bacteria, and viruses in marine samples. Curr. Protoc. Cytometry, 10 (1): 11.11.1–11.11.15.

    Google Scholar 

  • Meyer F, Paarmann D, D’Souza M, Olson R, Glass E, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards R A. 2008. The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics, 9: 386.

    Article  Google Scholar 

  • Mincer T J, Fenical W, Jensen P R. 2005. Culture–dependent and culture–independent diversity within the obligate marine actinomycete genus Salinispora. Appl. Environ. Microbiol., 71 (11): 7 019–7 028.

    Article  Google Scholar 

  • Mitchell J G. 2004. Rank–size analysis and vertical phytoplankton distribution patterns. In: Seuront L, Strutton P G eds. Handbook of Scaling Methods in Aquatic Ecology: Measurement, Analysis, Simulation. CRC Press, Boca Raton. p.257–278.

  • Mudge S, Moss M. 2008. State of the environment report for South Australia 2008. The State of Our Environment: Environmental Protection Authority, Adelaide. 311p.

    Google Scholar 

  • Newcombe R G. 1998. Improved confidence intervals for the difference between binomial proportions based on paired data. Statist. Med., 17 (22): 2 635–2 650.

    Article  Google Scholar 

  • Nieto J J, Fernández–Castillo R, Márquez M C, Ventosa A, Quesada E, Ruiz–Berraquero F. 1989. Survey of metal tolerance in moderately halophilic eubacteria. Appl. Environ. Microbiol., 55 (9): 2 385–2 390.

    Google Scholar 

  • Nogales B, Lanfranconi M P, Piña–Villalonga J M, Bosch R. 2011. Anthropogenic perturbations in marine microbial communities. FEMS Microbiol. Rev., 35 (2): 275–298.

    Article  Google Scholar 

  • Overbeek R, Begley T, Butler R M, Choudhuri J V, Chuang H Y, Cohoon M, de Crécy–Lagard V, Diaz N, Disz T, Edwards R, Fonstein R E M, Frank E D, Gerdes S, Glass E M, Goesmann A, Hanson A, Iwata–Reuyl D, Jensen R, Jamshidi N, Krause L, Kubal M, Larsen N, Linke B, McHardy A C, Meyer F, Neuweger H, Olsen G, Olson R, Osterman A, Portnoy V, Pusch G D, Rodionov D A, Rückert C, Steiner J, Stevens R, Thiele I, Vassieva O, Ye Y Z, Zagnitko O, Vonstein V. 2005. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res., 33 (17): 5 691–5 702.

    Article  Google Scholar 

  • Paez J G, Lin M, Beroukhim R, Lee J C, Zhao X J, Richter D J, Gabriel S, Herman P, Sasaki H, Altshuler D, Li C, Meyerson M, Sellers W R. 2004. Genome coverage and sequence fidelity of ϕ29 polymerase–based multiple strand displacement whole genome amplification. Nucleic Acids Res., 32 (9): e71.

    Article  Google Scholar 

  • Parks D H, Beiko R G. 2010. Identifying biologically relevant differences between metagenomic communities. Bioinformatics, 26 (6): 715–721.

    Article  Google Scholar 

  • Pǎsić L, Rodriguez–Mueller B, Martin–Cuadrado A B, Mira A, Rohwer F, Rodriguez–Valera F. 2009. Metagenomic islands of hyperhalophiles: the case of Salinibacter ruber. BMC Genomics, 10: 570.

    Article  Google Scholar 

  • Pedrós–Alió C, Calderón–Paz J I, MacLean M H, Medina G, Marrasé C, Gasol J M, Guixa–Boixereu N. 2000. The microbial food web along salinity gradients. FEMS Microbiol. Ecol., 32 (2): 143–155.

    Article  Google Scholar 

  • Pernthaler J. 2005. Predation on prokaryotes in the water column and its ecological implications. Nat. Rev. Microbiol., 3 (7): 537–546.

    Article  Google Scholar 

  • Persson B C. 1993. Modification of tRNA as a regulatory device. Mol. Microbiol., 8 (6): 1 011–1 016.

    Article  Google Scholar 

  • Raux E, Schubert H L, Warren M J. 2000. Biosynthesis of cobalamin (vitamin B12): a bacterial conundrum. Cell. Mol. Life Sci., 57 (13–14): 1 880–1 893.

    Google Scholar 

  • Reen F J, Almagro–Moreno S, Ussery D, Boyd E F. 2006. The genomic code: inferring Vibrionaceae niche specialization. Nat. Rev. Microbiol., 4 (9): 697–704.

    Article  Google Scholar 

  • Roberts M F. 2005. Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Syst., 1: 5.

    Article  Google Scholar 

  • Rodriguez–Brito B, Li L L, Wegley L, Furlan M, Angly F, Breitbart M, Buchanan J, Desnues C, Dinsdale E, Edwards R, Felts B, Haynes M, Liu H, Lipson D, Mahaffy J, Martin–Cuadrado A B, Mira A, Nulton J, Pašić L, Rayhawk S, Rodriguez–Mueller J, Rodriguez–Valera F, Salamon P, Srinagesh S, Thingstad T F, Tran T, Thurber R V, Willner D, Youle M, Rohwer F. 2010. Viral and microbial community dynamics in four aquatic environments. ISME J., 4 (6): 739–751.

    Article  Google Scholar 

  • Ruiz A, Franco J, Villate F. 1998. Microzooplankton grazing in the Estuary of Mundaka, Spain, and its impact on phytoplankton distribution along the salinity gradient. Aquat. Microb. Ecol., 14 (3): 281–288.

    Article  Google Scholar 

  • Rusch D B, Halpern A L, Sutton G, Heidelberg K B, Williamson S, Yooseph S, Wu D Y, Eisen J A, Hoffman J M, Remington K, Beeson K, Tran B, Smith H, Baden–Tillson H, Stewart C, Thorpe J, Freeman J, Andrews–Pfannkoch C, Venter J E, Li K, Kravitz S, Heidelberg J F, Utterback T, Rogers Y H, Falcón L I, Souza V, Bonilla–Rosso G, Eguiarte L E, Karl D M, Sathyendranath S, Platt T, Bermingham E, Gallardo V, Tamayo–Castillo G, Ferrari M R, Strausberg R L, Nealson K, Friedman R, Frazier M, Venter J C. 2007. The sorcerer II global ocean sampling expedition: northwest Atlantic through eastern Tropical Pacific. PLoS Biol., 5 (3): e77.

    Article  Google Scholar 

  • Sarikhan S, Azarbaijani R, Yeganeh L P, Fazeli A S, Amoozegar M A, Salekdeh G H. 2011. Draft genome sequence of Nesterenkonia sp. strain F, isolated from Aran–BidgolSalt Lake in Iran. J. Bacteriol., 193 (19): 5 580.

    Article  Google Scholar 

  • Schapira M, Buscot M J, Leterme S C, Pollet T, Chapperon C, Seuront L. 2009. Distribution of heterotrophic bacteria and virus–like particles along a salinity gradient in a hypersaline coastal lagoon. Aquat. Microb. Ecol., 54 (2): 171–183.

    Article  Google Scholar 

  • Seymour J R, Doblin M A, Jeffries T C, Brown M V, Newton K, Ralph P J, Baird M, Mitchell J G. 2012. Contrasting microbial assemblages in adjacent watermasses associated with the East Australian Current. Environ. Microbiol. Rep., 4 (5): 548–555.

    Article  Google Scholar 

  • Seymour J R, Humphreys W F, Mitchell J G. 2007. Stratification of the microbial community inhabiting an anchialine sinkhole. Aquat. Microb. Ecol., 50 (1): 11–24.

    Article  Google Scholar 

  • Smith R J, Jeffries T C, Roudnew B, Fitch A J, Seymour J R, Delpin M W, Newton K, Brown M H, Mitchell J G. 2012. Metagenomic comparison of microbial communities inhabiting confined and unconfined aquifer ecosystems. Environ. Microbiol., 14 (1): 240–253.

    Article  Google Scholar 

  • Stach E M, Bull A T. 2005. Estimating and comparing the diversity of marine actinobacteria. Antonie van Leeuwenhoek, 87 (1): 3–9.

    Article  Google Scholar 

  • Starr T J, Jones M E, Martinez D. 1957. The production of vitamin B 12–active substances by marine bacteria. Limnol. Oceanogr., 2 (2): 114–119.

    Article  Google Scholar 

  • Stevens H, Brinkhoff T, Rink B, Vollmers J, Simon M. 2007. Diversity and abundance of Gram positive bacteria in a tidal flat ecosystem. Environ. Microbiol., 9 (7): 1 810–1 822.

    Article  Google Scholar 

  • Strom S L. 2008. Microbial ecology of ocean biogeochemistry: a community perspective. Science, 320 (5879): 1 043–1 045.

    Article  Google Scholar 

  • Tamames J, Abellán J, Pignatelli M, Camacho A, Moya A. 2010. Environmental distribution of prokaryotic taxa. BMC Microbiol., 10: 85.

    Article  Google Scholar 

  • Thurber R V, Haynes M, Breitbart M, Wegley L, Rohwer F. 2009. Laboratory procedures to generate viral metagenomes. Nat. Protocols, 4 (4): 470–483.

    Article  Google Scholar 

  • Tourova T P, Spiridonova E M, Berg I A, Slobodova N V, Boulygina E S, Sorokin D Y. 2007. Phylogeny and evolution of the family Ectothiorhodospiraceae based on comparison of 16S rRNA, cbbL and nifH gene sequences. Int. J. Syst. Evol. Microbiol., 57 (10): 2 387–2 398.

    Article  Google Scholar 

  • Webster I T. 2005. An Overview of the Hydrodynamics of the Coorong and Murray Mouth. Technical Report No.#/2005. CSIRO: Water for a Healthy Country National Research Flagship. 33p.

    Google Scholar 

  • Wu Q L, Zwart G, Schauer M, Kamst–van Agterveld M P, Hahn M W. 2006. Bacterioplankton community composition along a salinity gradient of sixteen highmountain lakes located on the Tibetan Plateau, China. Appl. Environ. Microbiol., 72 (8): 5 478–5 485.

    Article  Google Scholar 

  • Yilmaz S, Allgaier M, Hugenholtz P. 2010. Multiple displacement amplification compromises quantitative analysis of metagenomes. Nat. Methods, 7 (12): 943–944.

    Article  Google Scholar 

  • Yokokawa T, Nagata T, Cottrell M T, Kirchman D L. 2004. Growth rate of the major phylogenetic bacterial groups in the Delaware estuary. Limnol. Oceanogr., 49 (5): 1 620–1 629.

    Article  Google Scholar 

  • Zar J H. 1996. Biostatistical Analysis. Prentice–Hall Inc., Upper Saddle River. 944p.

    Google Scholar 

Download references

Acknowledgement

The authors gratefully acknowledge B. Roudnew and T. Lavery for informative discussions, A. Burley and E. Alvino for editorial assistance. We sincerely thank A. Fitch from the School of Biological Sciences, Flinders University for technical support and guidance during laboratory work and S. Bailey and E. Ng from the Flow Cytometry Unit of the Flinders Medical Centre for providing technical support during flow cytometry sessions. We would like to especially thank the two anonymous reviewers whose comments and insights improved this manuscript. We also thank the Department of Environment and Natural Resources (DENR) for allowing us access to the Coorong National Park (permit number G25583-2). This research was supported by the Australian Research Council and by Flinders University. K. Newton was in recipient of a Flinders University Research Scholarship (FURS) at the time the research was undertaken.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kelly Newton.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Newton, K., Jeffries, T.C., Smith, R.J. et al. Taxonomic and metabolic shifts in the Coorong bacterial metagenome driven by salinity and external inputs. J. Ocean. Limnol. 36, 2033–2049 (2018). https://doi.org/10.1007/s00343-018-7387-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-018-7387-z

Keyword

Navigation