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5.1 Interactions among soil organisms

What types of interactions occur between organisms in soil?

There are many types of interactions between soil organisms which involve various mechanisms and physical structures. Many interactions are controlled by the physical way in which the organisms are in contact with each other. For example, some species of bacteria interact directly with other members of the same species via connecting threads or fibrils that attach the bacteria to one another. Alternatively, non-specific interactions commonly occur in wet environments where clumps of bacteria, algae and fungi of different kinds become combined in floating microbial mats or in biofilms. Although not physically connected in these dense aggregations, individuals of the same or different species can still influence each other.

Often the interactions between bacteria and fungi occur incidentally as a result of their close proximity. One organism may produce molecules that interfere directly with the growth of the other. For example, antibiotics produced by some bacteria can inhibit the growth of fungi. Other interactions may be beneficial for more than one organism. An example of this is a situation where cellulose-degrading bacteria release small carbon molecules that can be used by nitrogen-fixing bacteria. In return, the cellulose degrading bacteria receive nitrogen in a form that they can assimilate.

In many studies, interactions between soil organisms have been demonstrated. The studies that produced these outcomes have usually identified the effect of one organism on another. Fewer studies have identified the cause of the observed effect. The likely general mechanisms behind many interactions include changes in pH surrounding the organism or the grazing by soil animals on fungi and bacteria. Highly specific interactions also occur. For example, one bacterium may produce a molecule that is highly toxic to a closely related bacterium which is not toxic to more distantly related bacteria. Again, nematode-trapping fungi highlight the highly specialised interactions that occur among some soil organisms.

Interactions between earthworms and microorganisms

Earthworms can improve the chemical, physical and biological components of soil fertility by increasing microbial activity. Studies have shown that earthworm casts have higher concentrations of phosphorus, potassium, nitrogen and total carbon than the surrounding soil (Russell 1973). This is because microbial activity and subsequent mineralisation of organic matter increase with the passage of soil through the earthworm gut. In addition, the burrowing activities of earthworms improve the physical environment of the soil, facilitating beneficial microbial processes.

Generally, earthworms become active only in the soil if moisture is suitable and the supply of organic matter is sufficient, especially to satisfy their high requirement for nitrogen. Earthworms also have the potential to reduce root disease. For example, the incidence of wheat root-rot, caused by the fungus Gaeumannomyces graminis, is reduced in soils that contain earthworms (Stephens et al. 1994). In this study, the plants growing in soils with earthworms had lower disease ratings and higher shoot weights than plants growing in the absence of earthworms.

Interactions between cellulose degrading bacteria and nitrogen fixing bacteria during the degradation of straw

Non-symbiotic nitrogen-fixing bacteria are present in soil, as are organisms that produce the enzyme cellulase that is required during degradation of cellulose in plant material. Nitrogen-fixing bacteria use atmospheric nitrogen and require a source of carbon. Cellulose degrading bacteria obtain carbon from the decomposition of organic matter and require a source of nitrogen. Therefore, the potential exists for synergistic relationships to occur between nitrogen-fixing bacteria and cellulolytic bacteria. Nitrogen-fixing bacteria provide nitrogen to the cellulolytic bacteria which allows them to degrade plant material that is low in nitrogen (i.e. with a high C:N ratio).

An interesting interaction between a non-symbiotic nitrogen-fixing bacterium and a bacterium which can degrade cellulosewas investigated by Halsall and Gibson (1985). Nitrogen fixation by Azospirillum (measured as the amount of ethylene produced) was relatively low or even negligible when Cellulomonas (which can degrade cellulose) and Azospirillum (which can fix nitrogen) were grown alone. However, when they are grown together, nitrogen fixation increased. This occurred because Cellulomonas released nutrients from organic matter needed by Azospirillum to carry out nitrogen fixation. In turn, the nitrogen fixed by Azospirillum increased the activity of Cellulomonas. Nitrogen fixation was higher when carbon was provided in straw than in as pure cellulose. This was probably because straw contains nutrients not present pure cellulose even though cellulose is a major constituent of straw.

A similar effect was illustrated in a field study in which greater nitrogenase activity was associated with soil in which stubble was retained than in soil in which stubble was burned (Roper 1983). Where stubble was burnt, a gradual decline in nitrogenase activity was observed (this is an indicator of the relative quantity of nitrogen fixed in the two treatments). Where straw was incorporated into soil, nitrogenase activity remained higher than when straw was burnt. This is because the incorporation of the stubble into the soil adds a large amount of carbon for soil microorganisms to decompose. The energy released from its decomposition is utilised by other soil organisms, some of which are involved in nitrogen fixation.

Interactions between rhizobia during nodulation of clover

Many studies have shown that strains of rhizobia interact during the nodulation of legumes and that the strains of bacteria most effective at fixing nitrogen are not always those that form the majority of the nodules on the legumes. This was demonstrated in a study where the proportion of different strains of the bacteria, Rhizobium leguminosarum biovar trifolii, in an inocula was changed and the identity of the rhizobia in the nodules was determined (Triplett 1990). In this study, the strains of rhizobia differed in their ability to produce a toxin that inhibits the activity of rhizobial bacteria. They also differed in and in their sensitivity to the toxin. Three of the bacteria used were: (i) rhizobial strain TA1 which was sensitive to the toxin, (ii) rhizobial strain 2046 which was sensitive to the toxin, and (ii) rhizobial strain TA1 10-15 that produced the toxin but was also resistant to the toxin. TA1 10-15 was a genetically altered version of TA1 which had a gene for toxin production inserted into its DNA.

Before assessing the effect of the toxin-producing strain, the study examined the interaction between TA1 and 2046, which are both highly effective at nodulating clover roots and fixing nitrogen when present alone. As the relative amount of 2046 increased in the inoculum the ability of TA1 to form nodules decreased. Even when there were twice as many cells of TA1 than of 2046, TA1 only formed 40% of the nodules. Therefore, 2046 is more competitive than TA1 when they occur together and will form more nodules. Only when there are far more cells of TA1 than of 2046 did TA1 subdue its competitor and form most of the nodules.

In contrast, the genetically altered strain of TA1, strain TAI 10-15, was much more competitive against 2046. When there were only 1.6 times as many cells of TA1 10-15 than of 2046, 91% of the nodules were formed by TA1 10-15. Therefore, it appears that the insertion of the gene for toxin production into TA1 improved its competitiveness against strain 2046 because it was able to reduce the activity of 2046 (Table 82). However, when 2046 outnumbered TA1 10-15 by six times 2046 regained its competitive advantage. The toxin produced by TA1 10-15 was not enough to inhibit the activity of so many cells of 2046.

This experiment demonstrates the importance of specific characteristics of rhizobia to their competitiveness in forming nodules. Furthermore, it also shows that competitiveness alone is not sufficient to ensure nodulation. If less competitive bacteria are present in sufficiently high numbers in the soil, they may form the majority of the nodules.

Interactions between fungi during the colonisation of wood

A succession of fungi colonise dead wood lying on the forest floor during the slow process of degradation and recycling nutrients from the highly lignified wood material. The fungus Armillaria luteobubalina aggressively colonises old tree stumps. Inoculation of stumps of the tree Eucalyptus diversicolor with selected wood decaying fungi has been trialled as a means of controlling the spread of Armillaria. The ability of these fungi to prevent colonisation by Armillaria depended on which part of the stump they colonised. An interesting outcome of this investigation was that a naturally occurring fungus was highly effective in excluding Armillaria from the stumps (Pearce and Malajczuk 1990).

This study showed that one species of fungus may be excluded from a tree stump due to its colonisation by another fungus. The mechanism for this type of interaction may be related to differences in (i) growth rates of the fungi, leading to physical exclusion of a fungus by another fungus, (ii) the capacity of the fungi to form enzymes that help to degrade the stump material and releasing nutrients, (iii) the competitiveness of the fungi in obtaining nutrients released during mineralisation, and (iv) production of toxic molecules by the fungi.

Interactions between soil organisms in soil: the food-web

Bacteria, fungi and soil animals are all linked through the soil food-web (Dornbush et al. 2008). Food-web is a term that encompasses all the feeding relationships between organisms in an ecosystem. Soil organisms that degrade organic matter are the basis of the soil food-web as they provide all of the energy that flows through the rest of the web and these organisms interact in numerous ways. Soil animals feed on the bacteria and fungi that are involved in decomposition, hence there is a link between the numbers of bacteria and fungi in the soil and the numbers of animals. Different species of mites and nematodes have specific food preferences. For example, some mites eat other mites and collembolans, whereas other mites feed on bacteria or fungi. Similarly, some nematodes eat bacteria and others eat fungi.

Interactions between mycorrhizal fungi and small mammals in an Oregon coniferous forest

Although the focus of the above case studies has been on the interactions between soil organisms, interactions also occur between soil organisms and larger organisms. For example, the dependence of many tree species on mycorrhizal associations illustrates the links that occur between organisms of very different size in an ecosystem. Conversely, small mammals can be important for fungi as a way of dispersing fungal spores formed in underground fruiting structures. The spores within the sporocarps that are eaten by animals remain undamaged within faecal pellets and are dispersed throughout the forest. Studies of spores in faecal pellets and digestive tracts of small animals allow investigation of the species diversity of the fungi (Maser et al. 1978).

Four species of fungi were found in animals trapped in the forest site and at the edge of the forest, but only two species were present in animals trapped in the burned area. It is not known whether the animals discriminated by selecting different species of fungi. If there was no feeding discrimination, the study can be used to measure the abundance of sporocarps of fungi in different habitats. The lower diversity of fungi recorded in the burnt area is probably temporary.

How can land management influence interactions between soil organisms?

Soil disturbance influences the way that organisms interact with each other by altering the suitability of their environment for growth and reproduction. This can significantly change the dynamics of the food-web in soil, altering the availability of bacteria and fungi as food for soil fauna. Although our knowledge of the inter-connections among soil organisms is limited, the broad principles are well understood.

There is potential to either increase or decrease the intensity of interactions between organisms in field soils when a soil is disturbed for the purposes of land management. It is not simple to manage soils with the specific purpose of influencing one type of interaction. Changed soil conditions may eliminate one type of interaction between organisms, but simultaneously increase another. These interactions may have significant effects on plant growth if they involve the release of nutrients or growth of plant pathogens. Management practices need to be selected based on knowledge of more than one part of the soil microbial or animal community.

Summary Points (5.1)

• The diversity of organisms in the soil means that there are many interactions between them.

• Most of the mechanisms of interactions between organisms are not well understood, but there are examples of interactions which have been successfully investigated and explained.

• Many studies have demonstrated interactions between soil organisms, but have failed to identify the mechanism of the interaction.

• Interactions occur between both related and unrelated species of soil organisms.

• Interactions are not always of mutual benefit to the interacting organisms.

• There is a great potential for interactions to provide synergistic outcomes within the soil and land management practices can be selected to ensure that this occurs.

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