Biotopes on the scale of eukaryotic microbes

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For microorganisms, the scale of sizes and volumes is very different from what is familiar to us. This can lead to very different biotopes depending on the structure of the environment. Each will host its own flora and fauna of protists. For example, aquatic environments seem relatively homogeneous due to their fluidity. However, a structuring according to the depth is observed, even in low volume planes such as ponds. This structuring is related to the gradual decrease in brightness, increase in pressure and change in temperature often with cooling to the bottom. All these parameters also change according to the seasons. The presence of nutrients is also not homogeneous and can lead to additional structuring: heavier organic matter generally settles on the bottom. The very presence of photosynthetic organisms creates other nutritional gradients. For example, a microscopic unicellular algae will secrete organic matter. It can be the waste products of its metabolism, but also sugars that will passively diffuse through the membrane simply because they are concentrated inside the cell. This makes it possible to generate a micro-biotope around the algae, where various heterotrophs are present which feed on the organic matter it excretes (Figure 350). This example is a simplified version of a very common biotope: that of the immediate environment of a primary producer. In the case of a plant, the excretion of organic matter allows the development of a whole community of microorganisms on the leaves, a biotope called the phylloplane, and around the roots, an area called the rhizophere. This area is enriched with bacteria, fungi, small protozoa, mainly various amoebae and small animals such as nematodes.

Biotopes of restricted sizes are very numerous in nature and they will host specific protists. This is the case, for example, with the digestive tract of insects, such as that of termites. Termites are wood-consuming insects that recycle a good part of plant biomass, especially in intertropical regions. In fact, the enzymatic digestion of wood in the intestine is carried out by a whole community of prokaryotic and eukaryotic microorganisms more or less specific to each species. There are two main types. The first type of termites eat a broad diet and digest their food using Eumycota fungi. The second type, where e.g. Reticulitermes flavipes belongs, consume only wood (Figure 351). To make use of the wood, it is conventionally accepted that the termites of the second type possess flagellated symbionts, themselves associated with prokaryotes. Flagellates are essential for the digestion of cellulose which they transform into acetate, the source of carbon for the termite. A simple experiment consists in exposing the termites to a strong concentration of oxygen which kills the flagellates but leaves the termite alive, which dies a few days later… of hunger!

In Reticulitermes flavipes the posterior part of the intestine contains at least six species of Parabasalia flagellates, Ciliophora and about thirty eubacterial and Archean morphotypes. These morphotypes strongly underestimate the real biodiversity, which is more considerable when measured using PCR amplification and sequencing of ribosomal RNA. In Reticulitermes flavipes, Spirochaetes dominate the prokaryotic biomass since their rRNA represent half of the sequences. This is not the case with other termites; for example in Coptotermes formosanus, Bacteroidetes rRNA represent nearly three quarters of the sequences. In Reticulitermes flavipes, there are approximately 10,000 protozoa and 10 million prokaryotes per gut. Protists nevertheless represent 70% of the biomass. This can be estimated, for example, from the frequencies of the sequences of the various ribosomal RNAs and the known sizes of the various microbes. Free prokaryotes are rare and are therefore essentially symbionts of protozoa. Some are endobionts while others are epibionts attached to the surface of protozoa (Figure 48). They have a metabolic role (Figure 352) but also a role in the mobility of protists, by helping them to go up the flow of food so as not to be expelled with the faeces. The integration of partners is more or less extensive. For example, the symbiont of the Ciliophora Metopus contortus seems to have started a regressive evolution because it seems in part to have lost its cell wall.

This community of microorganism lives in syntrophy with the termite (Figure 352). The termite crushes the wood and its salivary glands secrete endo-cellulases which begin to break up cellulose in the anterior and middle part of the intestine (Figure 351). The termite can absorb glucose produced in the middle part of the intestine. Obviously, this glucose is not enough to ensure the survival of the insect. Protozoa also consume part of this cellulose, which they finish digesting in the posterior part of the intestine with the help of additional cellulase that they secrete. Their metabolism is anaerobic and they produce H₂ via their hydrogenosomes which function like that of Trichomonas vaginalis (Figure 31). Methanogenic and acetanogenic prokaryotes, whether they live harbored within protozoa or free, consume H₂, thus avoiding the inhibitory effect of too high a concentration of it. Prokaryotic metabolism results in the synthesis of acetate consumed by the termite and methane which will be excreted. The study of the characteristics of the digestive tract of termites is far from complete. We will retain that the intestine is not a homogeneous environment. In particular, there is a difference between the lumen and the edge of the tube (Figure 352). The lumen is an anoxic medium rich in H₂ while the edge is microoxic and poor in H₂. This is because oxygen arrives at the edge of the intestine via the termite respiratory system and diffuses through the wall of the intestine. Oxygen is reduced as it enters the lumen of the tube. This has an important impact on the metabolic flows inside the digestive tract and on the distribution of different microbes. The lumen is populated by flagellates which possess the hydrogenosomes and which produce hydrogen in the center of the digestive tract. This is used by their symbionts which include methanogenic archaea and acetanogenic eubacteria; acetanogens seem more present in the lumen and methanogens in the periphery.

Termite symbionts do not just help breaking down cellulose. They also participate in the degradation of lignin and nitrogen nutrition. Recently, it was shown that in Zootermopsis angusticollis, lignin is partially degraded during passage through the digestive tract. It is not yet known whether an Eumycota fungus participates in this degradation. However, it has been suggested that the wood-boring beetle Anoplophora glabripennis harbors a symbiotic fungus belonging to the genus Fusarium/Nectria which is involved in the degradation of lignin. Be that as it may, this property allows the termite to access the cellulose protected by the lignin. Similarly, it has just been shown by sequencing the genome of an endosymbiotic bacterium of the Parabasalid Pseudotrichonympha grassii, a flagellate associated with Coptotermes formosanus, that atmospheric nitrogen can be fixed during the symbiosis. This bacteria can also recycle the nitrogenous waste of the termite. This ensures a remarkable food autonomy for this species because obviously it can survive by consuming only wood! This termite is currently invading many regions.

In summary, there are very many biotopes of limited size which each have specific functions and inhabitants. In contrast to these restricted biotopes, there are some which cover large volumes or surfaces: soils of boreal, tropical or equatorial forests, soils of savannas, pelagic zone of the ocean, coastal bands… Each one results from the aggregation of microbiotopes, such as those described above. However, it is possible to study the collective effect of microorganisms, in particular eukaryotic microbes, on the large geochemical cycles for each of these large ecosystems.

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