Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Influence of historical inundation frequency on soil microbes (Cyanobacteria, Proteobacteria, Actinobacteria) in semi-arid floodplain wetlands

Tsuyoshi Kobayashi https://orcid.org/0000-0002-3641-4120 A E , Timothy J. Ralph B , Pranay Sharma C and Simon M. Mitrovic D
+ Author Affiliations
- Author Affiliations

A Science Division, Office of Environment and Heritage, PO Box 29, Lidcombe, NSW 1825, Australia.

B Department of Environmental Sciences, Faculty of Science and Engineering, Macquarie University, NSW 2109, Australia.

C School of Earth and Environmental Sciences, University of Adelaide, Adelaide, SA 5000, Australia.

D School of Life Sciences, University of Technology Sydney, PO Box 123, Broadway, NSW 2007, Australia.

E Corresponding author. Email: yoshi.kobayashi@environment.nsw.gov.au

Marine and Freshwater Research 71(5) 617-625 https://doi.org/10.1071/MF18468
Submitted: 6 December 2018  Accepted: 30 March 2019   Published: 31 May 2019

Abstract

Cyanobacteria and other microbes are important moderators of biogeochemical processes in semi-arid floodplain wetlands with varying inundation regimes. Inundation is a key environmental driver for floodplain biological communities. Little is known about the effect of historical inundation frequency on the spatial abundance of floodplain–wetland Cyanobacteria and other microbes. In this study, soil samples were collected at two locations with a gradient of low-to-high inundation frequency in the Macquarie Marshes, south-east Australia. We used high-throughput sequencing to estimate the proportional abundance of the soil Cyanobacteria and other dominant microbes, targeting the bacterial 16S rRNA gene. Of the microbes recovered, Cyanobacteria constituted proportionally a minor component, relative to other dominant phyla like Proteobacteria and Actinobacteria. Linear regression (generalised least-squares) models accounting for spatial autocorrelation showed that historical inundation frequency had no significant effect on the proportional abundance of Cyanobacteria at both wetlands studied. However, inundation frequency had a significant positive effect on the proportional abundance of Proteobacteria and a significant negative effect on the proportional abundance of Actinobacteria. Cyanobacteria seem to occupy a different hydrological niche from Proteobacteria and Actinobacteria in semi-arid floodplain wetlands, suggesting taxon-dependent response of floodplain microbial communities to varying inundation regimes and associated soil conditions in those environments.

Additional keywords: inundation gradient, wetlands in drylands.


References

Agrawal, S. C., and Singh, V. (2002). Viability of dried filaments, survivability and reproduction under water stress, and survivability following heat and UV exposure in Lyngbya martensiana, Oscillatoria agardhii, Nostoc calcicola, Hormidium fluitans, Spirogyra sp. and Vaucheria geminata. Folia Microbiologica 47, 61–67.
Viability of dried filaments, survivability and reproduction under water stress, and survivability following heat and UV exposure in Lyngbya martensiana, Oscillatoria agardhii, Nostoc calcicola, Hormidium fluitans, Spirogyra sp. and Vaucheria geminata.Crossref | GoogleScholarGoogle Scholar | 11980272PubMed |

Akaike, H. (1974). A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716–723.
A new look at the statistical model identification.Crossref | GoogleScholarGoogle Scholar |

Argiroff, W. A., Zak, D. R., Lanser, C. M., and Wiley, M. J. (2017). Microbial community functional potential and composition are shaped by hydrologic connectivity in riverine floodplain soils. Microbial Ecology 73, 630–644.
Microbial community functional potential and composition are shaped by hydrologic connectivity in riverine floodplain soils.Crossref | GoogleScholarGoogle Scholar | 27807645PubMed |

Baldwin, D. S., and Mitchell, A. M. (2000). The effects of drying and re-flooding on the sediment and soil nutrient dynamics of lowland river–floodplain systems: a synthesis. Regulated Rivers: Research and Management 16, 457–467.
The effects of drying and re-flooding on the sediment and soil nutrient dynamics of lowland river–floodplain systems: a synthesis.Crossref | GoogleScholarGoogle Scholar |

Barinova, S., Nevo, E., and Bragina, T. (2011). Ecological assessment of wetland ecosystems of northern Kazakhstan on the basis of hydrochemistry and algal biodiversity. Acta Botanica Croatica 70, 215–244.
Ecological assessment of wetland ecosystems of northern Kazakhstan on the basis of hydrochemistry and algal biodiversity.Crossref | GoogleScholarGoogle Scholar |

Beguería, S., and Pueyo, Y. (2009). A comparison of simultaneous autoregressive and generalized least squares models for dealing with spatial autocorrelation. Global Ecology and Biogeography 18, 273–279.
A comparison of simultaneous autoregressive and generalized least squares models for dealing with spatial autocorrelation.Crossref | GoogleScholarGoogle Scholar |

Burnham, K. P., and Anderson, D. R. (2002). ‘Model Selection and Multimodel Inference: A Practical Information-Theoretical Approach’, 2nd edn. (Springer-Verlag: New York, NY, USA.)

Bush, T., Diao, M., Allen, R. J., Sinnige, R., Muyzer, G., and Huisman, J. (2017). Oxic–anoxic regime shifts mediated by feedbacks between biogeochemical processes and microbial community dynamics. Nature Communications 8, 789.
Oxic–anoxic regime shifts mediated by feedbacks between biogeochemical processes and microbial community dynamics.Crossref | GoogleScholarGoogle Scholar | 28986518PubMed |

Canfield, D. E., and Des Marais, D. J. (1993). Biogeochemical cycles of carbon, sulfur, and free oxygen in a microbial mat. Geochimica et Cosmochimica Acta 57, 3971–3984.
Biogeochemical cycles of carbon, sulfur, and free oxygen in a microbial mat.Crossref | GoogleScholarGoogle Scholar | 11537735PubMed |

Dale, M. R., and Fortin, M. J. (2014). ‘Spatial Analysis: A Guide for Ecologists’, 2nd edn. (Cambridge University Press: Cambridge, UK.)

Draper, N., and Smith, H. (1981). ‘Applied Regression Analysis’, 2nd edn. (Wiley: New York, NY, USA.)

Galloway, J. N., Dentener, F. J., Capone, D. G., Boyer, E. W., Howarth, R. W., Seitzinger, S. P., Asner, G. P., Cleveland, C. C., Green, P. A., Holland, E. A., and Karl, D. M. (2004). Nitrogen cycles: past, present, and future. Biogeochemistry 70, 153–226.
Nitrogen cycles: past, present, and future.Crossref | GoogleScholarGoogle Scholar |

Green, A. J., Alcorlo, P., Peeters, E. T., Morris, E. P., Espinar, J. L., Bravo-Utrera, M. A., Bustamante, J., Díaz-Delgado, R., Koelmans, A. A., Mateo, R., and Mooij, W. M. (2017). Creating a safe operating space for wetlands in a changing climate. Frontiers in Ecology and the Environment 15, 99–107.
Creating a safe operating space for wetlands in a changing climate.Crossref | GoogleScholarGoogle Scholar |

Guindon, S., and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.
A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.Crossref | GoogleScholarGoogle Scholar | 14530136PubMed |

Hartman, W. H., Richardson, C. J., Vilgalys, R., and Bruland, G. L. (2008). Environmental and anthropogenic controls over bacterial communities in wetland soils. Proceedings of the National Academy of Sciences of the United States of America 105, 17842–17847.
Environmental and anthropogenic controls over bacterial communities in wetland soils.Crossref | GoogleScholarGoogle Scholar | 19004771PubMed |

Huisman, J., Codd, G. A., Paerl, H. W., Ibelings, B. W., Verspagen, J. M., and Visser, P. M. (2018). Cyanobacterial blooms. Nature Reviews. Microbiology 16, 471–483.
Cyanobacterial blooms.Crossref | GoogleScholarGoogle Scholar | 29946124PubMed |

Hurvich, C. M., and Tsai, C.-L. (1989). Regression and time series model selection in small samples. Biometrika 76, 297–307.
Regression and time series model selection in small samples.Crossref | GoogleScholarGoogle Scholar |

John, J., and Kemp, A. (2006). Cyanobacterial blooms in the wetlands of the Perth region, taxonomy and distribution: an overview. Journal of the Royal Society of Western Australia 89, 51–56.

Kaplan-Levy, R. N., Hadas, O., Summers, M. L., Rücker, J., and Sukenik, A. (2010). Akinetes: dormant cells of Cyanobacteria. In ‘Dormancy and Resistance in Harsh Environments, Topics in Current Genetics 21’. (Eds E. Lubzens, J. Cerdà, and M. S. Clark.) pp. 5–27. (Springer-Verlag: Berlin, Germany.)

Kersters, K., De Vos, P., Gillis, M., Swings, J., Vandamme, P., and Stackebrandt, E. (2006). Introduction to the Proteobacteria. In ‘The Prokaryotes’. (Eds M. Dworkin, S. Falkow, E. Rosenberg, K. H. Schleifer, and E. Stackebrandt.) pp. 3–37. (Springer: New York, NY, USA.)

Kobayashi, T., Ryder, D. S., Gordon, G., Shannon, I., Ingleton, T., Carpenter, M., and Jacobs, S. J. (2009). Short-term response of nutrients, carbon and planktonic microbial communities to floodplain wetland inundation. Aquatic Ecology 43, 843–858.
Short-term response of nutrients, carbon and planktonic microbial communities to floodplain wetland inundation.Crossref | GoogleScholarGoogle Scholar |

Kühn, I. (2007). Incorporating spatial autocorrelation may invert observed patterns. Diversity & Distributions 13, 66–69.

Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007). Clustal W and clustal X version 2.0. Bioinformatics 23, 2947–2948.
Clustal W and clustal X version 2.0.Crossref | GoogleScholarGoogle Scholar | 17846036PubMed |

Lewin, G. R., Carlos, C., Chevrette, M. G., Horn, H. A., McDonald, B. R., Stankey, R. J., Fox, B. G., and Currie, C. R. (2016). Evolution and ecology of actinobacteria and their bioenergy applications. Annual Review of Microbiology 70, 235–254.
Evolution and ecology of actinobacteria and their bioenergy applications.Crossref | GoogleScholarGoogle Scholar | 27607553PubMed |

Ligi, T., Oopkaup, K., Truu, M., Preem, J. K., Nõlvak, H., Mitsch, W. J., Mander, Ü., and Truu, J. (2014). Characterization of bacterial communities in soil and sediment of a created riverine wetland complex using high-throughput 16S rRNA amplicon sequencing. Ecological Engineering 72, 56–66.
Characterization of bacterial communities in soil and sediment of a created riverine wetland complex using high-throughput 16S rRNA amplicon sequencing.Crossref | GoogleScholarGoogle Scholar |

Marín, I. (2015). Proteobacteria. In ‘Encyclopedia of Astrobiology’, 2nd edn. (Eds M. Gargaud, W. M. Irvine, R. Amils, H. J. Cleaves II, D. Pinti, J. Cernicharo Quintanilla, D. Rouan, T. Spohn, S. Tirard, and M. Viso.) pp. 2036–2037. (Springer: Heidelberg, Germany.)

Mitsch, W. J., and Gosselink, J. G. (2007). ‘Wetlands’, 4th edn. (Wiley: Hoboken, NJ, USA.)

Moran, P. A. (1950). Notes on continuous stochastic phenomena. Biometrika 37, 17–23.
Notes on continuous stochastic phenomena.Crossref | GoogleScholarGoogle Scholar | 15420245PubMed |

Murphy, T., Lawson, A., Nalewajko, C., Murkin, H., Ross, L., Oguma, K., and McIntyre, T. (2000). Algal toxins – initiators of avian botulism? Environmental Toxicology: an International Journal 15, 558–567.
Algal toxins – initiators of avian botulism?Crossref | GoogleScholarGoogle Scholar |

Ocock, J. F., Kingsford, R. T., Penman, T. D., and Rowley, J. J. (2016). Amphibian abundance and detection trends during a large flood in a semi-arid floodplain wetland. Herpetological Conservation and Biology 11, 408–425.

Padan, E. (1979). Facultative anoxygenic photosynthesis in cyanobacteria. Annual Review of Plant Physiology 30, 27–40.
Facultative anoxygenic photosynthesis in cyanobacteria.Crossref | GoogleScholarGoogle Scholar |

Paerl, H. W., Hall, N. S., and Calandrino, E. S. (2011). Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. The Science of the Total Environment 409, 1739–1745.
Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change.Crossref | GoogleScholarGoogle Scholar | 21345482PubMed |

Peipoch, M., Jones, R., and Valett, H. M. (2015). Spatial patterns in biofilm diversity across hierarchical levels of river–floodplain landscapes. PLoS One 10, e0144303.
Spatial patterns in biofilm diversity across hierarchical levels of river–floodplain landscapes.Crossref | GoogleScholarGoogle Scholar | 26630382PubMed |

Peralta, A. L., Ludmer, S., Matthews, J. W., and Kent, A. D. (2014). Bacterial community response to changes in soil redox potential along a moisture gradient in restored wetlands. Ecological Engineering 73, 246–253.
Bacterial community response to changes in soil redox potential along a moisture gradient in restored wetlands.Crossref | GoogleScholarGoogle Scholar |

Ralph, T. J., and Hesse, P. P. (2010). Downstream hydrogeomorphic changes along the Macquarie River, southeastern Australia, leading to channel breakdown and floodplain wetlands. Geomorphology 118, 48–64.
Downstream hydrogeomorphic changes along the Macquarie River, southeastern Australia, leading to channel breakdown and floodplain wetlands.Crossref | GoogleScholarGoogle Scholar |

Ralph, T. J., Kobayashi, T., García, A., Hesse, P. P., Yonge, D., Bleakley, N., and Ingleton, T. (2011). Paleoecological responses to avulsion and floodplain evolution in a semiarid Australian freshwater wetland. Australian Journal of Earth Sciences 58, 75–91.
Paleoecological responses to avulsion and floodplain evolution in a semiarid Australian freshwater wetland.Crossref | GoogleScholarGoogle Scholar |

Ralph, T. J., Hesse, P. P., and Kobayashi, T. (2016). Wandering wetlands: spatial patterns of historical channel and floodplain change in the Ramsar-listed Macquarie Marshes, Australia. Marine and Freshwater Research 67, 782–802.
Wandering wetlands: spatial patterns of historical channel and floodplain change in the Ramsar-listed Macquarie Marshes, Australia.Crossref | GoogleScholarGoogle Scholar |

Rejmánková, E., Komárek, J., and Komárková, J. (2004). Cyanobacteria – a neglected component of biodiversity: patterns of species diversity in inland marshes of northern Belize (Central America). Diversity & Distributions 10, 189–199.
Cyanobacteria – a neglected component of biodiversity: patterns of species diversity in inland marshes of northern Belize (Central America).Crossref | GoogleScholarGoogle Scholar |

Rogers, K., and Ralph, T. J. (2011). Impacts of hydrological changes on floodplain wetland biota. In ‘Floodplain Wetland Biota in the Murray–Darling Basin: Water and Habitat Requirements’. (Eds K. Rogers and T. J. Ralph.) pp. 311–325. (CSIRO Publishing: Melbourne, Vic., Australia.)

Shi, L., Cai, Y., Chen, Z., Zhou, Y., Li, P., and Kong, F. (2010). Diversity and abundance of aerobic anoxygenic phototrophic bacteria in two cyanobacterial bloom-forming lakes in China. International Journal of Limnology 46, 233–239.
Diversity and abundance of aerobic anoxygenic phototrophic bacteria in two cyanobacterial bloom-forming lakes in China.Crossref | GoogleScholarGoogle Scholar |

Smith, M. J., Schreiber, E. S. G., Kohout, M., Ough, K., Lennie, R., Turnbull, D., Jin, C., and Clancy, T. (2007). Wetlands as landscape units: spatial patterns in salinity and water chemistry. Wetlands Ecology and Management 15, 95–103.
Wetlands as landscape units: spatial patterns in salinity and water chemistry.Crossref | GoogleScholarGoogle Scholar |

Taranu, Z. E., Gregory-Eaves, I., Steele, R. J., Beaulieu, M., and Legendre, P. (2017). Predicting microcystin concentrations in lakes and reservoirs at a continental scale: a new framework for modelling an important health risk factor. Global Ecology and Biogeography 26, 625–637.
Predicting microcystin concentrations in lakes and reservoirs at a continental scale: a new framework for modelling an important health risk factor.Crossref | GoogleScholarGoogle Scholar |

Thomas, R. F., Kingsford, R. T., Lu, Y., and Hunter, S. J. (2011). Landsat mapping of annual inundation (1979–2006) of the Macquarie Marshes in semi-arid Australia. International Journal of Remote Sensing 32, 4545–4569.
Landsat mapping of annual inundation (1979–2006) of the Macquarie Marshes in semi-arid Australia.Crossref | GoogleScholarGoogle Scholar |

Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.Crossref | GoogleScholarGoogle Scholar | 7984417PubMed |

Tockner, K., and Stanford, J. A. (2002). Riverine flood plains: present state and future trends. Environmental Conservation 29, 308–330.
Riverine flood plains: present state and future trends.Crossref | GoogleScholarGoogle Scholar |

Tsygankov, A. A. (2007). Nitrogen-fixing cyanobacteria: a review. Applied Biochemistry and Microbiology 43, 250–259.
Nitrogen-fixing cyanobacteria: a review.Crossref | GoogleScholarGoogle Scholar |

Verhoeven, J. T. A., Beltman, B., Whigham, D. F., and Bobbink, R. (2006). Wetland functioning in a changing world: implications for natural resources management. In ‘Wetlands and Natural Resource Management’. (Eds J. T. A. Verhoeven, B. Beltman, R. Bobbink, and D. F. Whigham.) pp. 1–12. (Springer: Berlin, Germany.)

Ward, M. D., and Gleditsch, K. S. (2008). ‘Spatial Regression Models.’ (SAGE Publications: Los Angeles, CA, USA.)

Warton, D. I., and Hui, F. K. (2011). The arcsine is asinine: the analysis of proportions in ecology. Ecology 92, 3–10.
The arcsine is asinine: the analysis of proportions in ecology.Crossref | GoogleScholarGoogle Scholar | 21560670PubMed |

Wilson, J. S., Baldwin, D. S., Rees, G. N., and Wilson, B. P. (2011). The effects of short-term inundation on carbon dynamics, microbial community structure and microbial activity in floodplain soil. River Research and Applications 27, 213–225.
The effects of short-term inundation on carbon dynamics, microbial community structure and microbial activity in floodplain soil.Crossref | GoogleScholarGoogle Scholar |