Spatial and Temporal Fluctuations in Bacteria, Microfauna and Mineral Nitrogen in Response to a Nutrient Impulse in Soil
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Spatial and temporal fluctuations in bacteria, microfauna and mineral nitrogen in response to a nutrient impulse in soil Vladimir Viktorovich Zelenev Promotor: Prof. Dr. Ir. Ariena H.C. van Bruggen Hoogleraar in Biologische Bedrijfssystemen Wageningen Universiteit Co-promotor: Dr. Alexander M. Semenov Senior Research Scientist in the Department of Microbiology Moscow State University Promotiecommissie: Prof. Dr. Lijbert Brussaard (Wageningen Universiteit) Prof. Dr. Peter C. de Ruiter (Universiteit Utrecht) Prof. Dr. J. Dick van Elsas (Rijksuniversiteit Groningen) Dr. Ir. Peter A. Leffelaar (Wageningen Universiteit) Dit onderzoek is uitgevoerd binnen de C.T. de Wit Onderzoekschool ‘Productie Ecologie en Beheer van Natuurlijke Hulpbronnen’. Vladimir V. Zelenev Spatial and temporal fluctuations in bacteria, microfauna and mineral nitrogen in response to a nutrient impulse in soil Proefschrift ter verkrijging van de graad van doctor op gezag van de rector magnificus van Wageningen Universiteit, Prof. Dr. Ir. L. Speelman in het openbaar te verdedigen op vrijdag 19 maart 2004 des namiddags te 13:30 uur in de Aula Bibliographic data Zelenev, V.V. (2004) Spatial and temporal fluctuations in bacteria, microfauna and mineral nitrogen in response to a nutrient impulse in soil. PhD Thesis Wageningen University, The Netherlands With summaries in English, Russian, and Dutch – x + 190 pp. Key words: soil bacterial populations, CFU, direct counts, rhizosphere, root, copiotrophs, oligotrophs, trophic groups of bacteria, distribution, disturbance, oscillations, fluctuations, short-term wave-like dynamics, fresh plant residues, debris, substrate, mineral nitrogen release, nematodes, protozoa, predator-prey relations, soil food web, harmonics, Fourier analysis, modeling, simulation. ISBN 90-5808-988-6 To Ariena, Alexander, my grandmother Irina, my mother Roza, my father Viktor, my sister Nadiusha for inspiration, concern, patience, and love Abstract Fluctuations of bacterial populations can be observed when frequent and sufficiently long series of samples are obtained for direct microscopic or plate counts of bacteria. Fluctuations in bacterial numbers are especially noticeable after some disturbance of soil such as substrate addition. However, very seldom were bacterial fluctuations subjected to proper statistical analysis to detect significant periodical components in the data. In this thesis, bacterial dynamics and distributions were investigated in short-term (1 month) controlled experiments for rhizosphere and bulk soil after substrate input from plant roots and fresh plant debris, respectively. By using harmonics analysis, significant wave-like oscillations in bacterial numbers were detected along wheat roots and over time after clover-grass incorporation into soil. Oscillations were not related to numbers of lateral roots, soil moisture, mineral nitrogen concentrations, pH or redox potential. Soil fauna was not monitored in the rhizosphere experiments. In clover-grass experiments, nematode populations and composition were monitored daily, while protozoa were enumerated occasionally. Bacterial feeding nematode populations did not oscillate, but daily changes in their numbers did oscillate with a frequency similar to that of bacterial oscillations. Short-term oscillating dynamics of bacterial populations were simulated in two mechanistic models: “BACWAVE” to simulate the wave-like distribution of copiotrophic and oligotrophic bacterial populations along roots and “BACWAVE-WEB” to simulate wave-like oscillations of 3 trophic groups of bacteria (copiotrophic, hydrolytic, and oligotrophic) and their predators (protozoa and nematodes) over time after incorporation of plant residues into soil. In both models relative growth and death rates were non-linearly related to readily utilizable substrate concentrations, so that the cross-over point of the growth and death rate curves occurred at realistic substrate concentrations. A good fit was obtained to the observed data. Mineral nitrogen release was also modeled satisfactorily with “BACWAVE- WEB”. Virtual experiments suggested that substrate-bacteria interactions are more important for regulation of bacterial oscillations than predator-prey interactions, and that regulation by protozoa was more influential than that by nematodes. Release of mineral nitrogen was primarily determined by bacteria, and to a lesser extent by predators. Oligotrophic bacteria played an important role in stimulating hydrolytic enzyme production and moderating bacterial fluctuations. The “BACWAVE-WEB” model has good potential to predict responses if microbial communities to a disturbance, which could be used to characterize soil health. Contents Abstract Contents Chapter 1 Introduction and overview 1 Chapter 2 Moving waves of bacterial populations and total organic carbon along roots of 17 wheat Chapter 3 “BACWAVE”, a spatial-temporal model for traveling waves of bacterial 37 populations in response to a moving carbon source in soil Chapter 4 Modeling wave-like dynamics of oligotrophic and copiotrophic bacteria along 57 wheat roots in response to nutrient input from a growing root tip Chapter 5 Short-term wave-like dynamics of bacterial populations in response to nutrient 75 input from fresh plant residues Chapter 6 Daily changes in bacterial-feeding nematode populations oscillate with similar 93 periods as bacterial populations after a nutrient impulse in soil Chapter 7 “BACWAVE-WEB”, a simulation model for oscillating dynamics of 113 bacterial populations and their predators in response to fresh organic matter added to soil Chapter 8 General discussion 163 Summary 171 Резюме 175 Samenvatting 181 Acknowledgements 187 Biography 189 Chapter 1 Introduction and overview 1 Introduction and overview Cycles and fluctuations Living nature operates in cycles, in particular daily, seasonal and annual cycles, as influenced by corresponding oscillations in temperature, humidity and light. There are also strong influences of available sources of carbon and other biogenic elements on living nature. The main cycle of living organisms is birth and death. Birth and death rates are not only determined by availability of resources but also by competition for these sources, predation and parasitism. Under non-limiting environmental conditions, including nutrients or waste products, there would be unlimited growth and random death or death due to ageing. Under limiting conditions, however, more or less synchronic birth and death cycles can be expected at small spatial scales. Besides these regular cycles, irregular fluctuations in populations have frequently been observed. Unusual or irregular data may have been ignored in the past, but in the last three decades, ecologists have tried to bring order in these data. Temporal and spatial fluctuations have been analyzed and modeled extensively for mammals, insects, and plants (Virtanen et al., 2002; Turchin et al., 1999), but less frequently for microorganisms (Zvyagintsev and Golimbet.,1983; Zvyagintsev, 1987; Vayenas and Pavlou, 2001). The population dynamics of macroscopic (and to a lesser extent microscopic) organisms has been described as periodic, wave-like or chaotic using deterministic analytical models (Poole, 1977; Vayenas and Pavlou, 2001). Such patterns might have been ascribed to underlying physical, chemical or nutritional factors in the past, but could be totally explained by inter-species interactions (Hassell et al., 1994; Gilligan 1995). Spatially chaotic patterns can revert to regular, wave-like patterns as a result of a perturbation in the form of ‘pulse’ or ‘wave’ control (Doebeli and Ruxton, 1997). Destabilization of spatially homogeneous equilibria can lead to a new steady state behaving as a standing spatial wave of population abundances. Thus, stable pattern formation can arise after a disturbance in both multiple- species and single-species models (Doebeli and Ruxton, 1998). Fluctuations in microbial populations There are many publications in which fluctuations in microbial populations are apparent from the figures, but in most cases, no special attention was paid to these fluctuations. When the authors did investigate the fluctuations and tried to explain them, attempts were sometimes made to relate the observed fluctuations directly to similar fluctuations in environmental conditions or such observations were left without any explanation. The data sets were often limited and, with some exceptions (Aristovskaya et al., 1977), statistical analyses were usually not carried out. When oscillations in microbial populations were intentionally studied, these were mostly studied in the context of predator – prey or host – parasite interactions (Gilligan, 1995; Doebeli and Ruxton, 1998). Microbial dynamics can be classified into three basic types: (1) seemingly random, (2) apparently fluctuating with changes in environmental factors, (3) more or less regular oscillations. Moreover, fluctuations can dampen and reach a plateau or can continue as long as observations are carried out. 2 The ability to detect microbial fluctuations depends very much on the frequency and duration of the observations. Regular oscillations become especially noticeable when population densities are measured frequently, for example every day. This thesis will be focused on revealing more or less regular oscillations over time and in space, and on the processes that are involved in regulation of these oscillations. Thus, microbial cell cycles based on circadian rhythms or influenced by seasons will