Mutualisms involving gut inhabitants

Most of the mutualisms discussed so far have depended on patterns of behavior, where neither species lives entirely 'within' its partner. In many other mutualisms, one of the partners is a unicellular eukaryote or bacterium that is integrated more or less permanently into the body cavity or even the cells of its multicellular partner. The microbiota occupying parts of various animals' alimentary canals are the best known extracellular symbionts.

13.5.1 Vertebrate guts

The crucial role of microbes in the digestion of cellulose by vertebrate herbivores has long been appreciated, but it now appears that the gastrointestinal tracts of all vertebrates are populated by a mutualistic microbiota (reviewed in Stevens & Hume, 1998). Protozoa and fungi are usually present but the major contributors to these 'fermentation' processes are bacteria. Their diversity is greatest in regions of the gut where the pH is relatively neutral and food retention times are relatively long. In small mammals (e.g. rodents, rabbits and hares) the cecum is the main fermentation chamber, whereas in larger nonruminant mammals such as horses the colon is the main site, as it is in elephants, which, like rabbits, practice coprophagy (consume their own feces) (Figure 13.10). In ruminants, like cattle and sheep, and in kangaroos and other marsupials, fermentation occurs in specialized stomachs.

The basis of the mutualism is straightforward. The microbes receive a steady flow of substrates for growth in the form of food that has been eaten, chewed and partly homogenized. They live within a chamber in which pH and, in endotherms, temperature are regulated and anaerobic conditions are maintained. The vertebrate hosts, especially the herbivores, receive nutrition from food that they would otherwise find, literally, indigestible. The bacteria produce short-chain fatty acids (SCFAs) by fermentation of the host's dietary cellulose and starches and of the endogenous

Figure 13.10 The digestive tracts of herbivorous mammals are commonly modified to provide fermentation chambers inhabited by a rich fauna and flora or microbes. (a) A rabbit, with a fermentation chamber in the expanded cecum. (b) A zebra, with fermentation chambers in both the cecum and colon. (c) A sheep, with foregut fermentation in an enlarged portion of the stomach, rumen and reticulum. (d) A kangaroo, with an elongate fermentation chamber in the proximal portion of the stomach. (After Stevens & Hume, 1998.)

Foregut Fermentation Rabbits

Figure 13.10 The digestive tracts of herbivorous mammals are commonly modified to provide fermentation chambers inhabited by a rich fauna and flora or microbes. (a) A rabbit, with a fermentation chamber in the expanded cecum. (b) A zebra, with fermentation chambers in both the cecum and colon. (c) A sheep, with foregut fermentation in an enlarged portion of the stomach, rumen and reticulum. (d) A kangaroo, with an elongate fermentation chamber in the proximal portion of the stomach. (After Stevens & Hume, 1998.)

Species

Function

Products

Bacteroides succinogenes

C, A

F, A,

S

Ruminococcus albus

C, X

F, A,

E, H, C

R. flavefaciens

C, X

F, A,

S, H

Butyrivibrio fibrisolvens

C, X, PR

F, A,

L, B, E, H, C

Clostridium lochheadii

C, PR

F, A,

B, E, H, C

Streptococcus bovis

A, SS, PR

L, A,

F

B. amylophilus

A, P, PR

F, A,

S

B. ruminicola

A, X, P, PR

F, A,

P, S

Succinimonas amylolytica

A, D

A, S

Selenomonas ruminantium

A, SS, GU, LU, PR

A, L,

P, H, C

Lachnospira multiparus

P, PR, A

F, A,

E, L, H, C

Succinivibrio dextrinosolvens

P, D

F, A,

L, S

Methanobrevibacter ruminantium

M, HU

M

Methanosarcina barkeri

M, HU

M, C

Spirochete species

P, SS

F, A,

L, S, E

Megasphaera elsdenii

SS, LU

A, P,

B, V, CP, H, C

Lactobacillus sp.

SS

L

Anaerovibrio lipolytica

L, GU

A, P,

S

Eubacterium ruminantium

SS

F, A,

B, C

Table 13.1 A number of the bacterial species of the rumen, illustrating their wide range of functions and the wide range of products that they generate. (After Allison, 1984; Stevens & Hume, 1998.)

Functions: A, amylolytic; C, cellulolytic; D, dextrinolytic; GU, glycerol utilizing; HU, hydrogen utilizer; L, lipolytic; LU, lactate utilizing; M, methanogenic; P, pectinolytic; PR, proteolytic; SS, major soluble sugar fermenter; X, xylanolytic.

Products: A, acetate; B, butyrate; C, carbon dioxide; CP, caproate; E, ethanol; F, formate; H, hydrogen; L, lactate; M, methane P, propionate; S, succinate; V, valerate;.

Table 13.1 A number of the bacterial species of the rumen, illustrating their wide range of functions and the wide range of products that they generate. (After Allison, 1984; Stevens & Hume, 1998.)

carbohydrates contained in host mucus and sloughed epithelial cells. SCFAs are often a major source of energy for the host; for example, they provide more than 60% of the maintenance energy requirements for cattle and 29-79% of those for sheep (Stevens & Hume, 1998). The microbes also convert nitrogenous compounds (amino acids that escape absorption in the midgut, urea that would otherwise be excreted by the host, mucus and sloughed cells) into ammonia and microbial protein, conserving nitrogen and water; and they synthesize B vitamins. The microbial protein is useful to the host if it can be digested - in the intestine by foregut fermenters and following coprophagy in hindgut fermenters - but ammonia is usually not useful and may even be toxic to the host.

13.5.2 Ruminant guts

The stomach of ruminants comprises a three-part forestomach (rumen, reticulum and omasum) followed by an enzyme-secreting abomasum that is similar to the whole stomach of most other vertebrates. The rumen and reticulum are the main sites of fermentation, and the omasum serves largely to transfer material to the abomasum. Only particles with a volume of about 5 |ll or less can pass from the reticulum into the omasum; the animal regurgitates and rechews the larger particles (the pro cess of rumination). Dense populations of bacteria (10 10-1011 ml-1) and protozoa (105-106 ml-1 but occupying a similar volume to the bacteria) are present in the rumen. The bacterial communities of the rumen are composed almost wholly of obligate anaerobes - many are killed instantly by exposure to oxygen -but they perform a wide variety of functions (subsist on a wide variety of substrates) and generate a wide range of products (Table 13.1). Cellulose and other fibers are the important constituents of the ruminant's diet, and the ruminant itself lacks the enzymes to digest these. The cellulolytic activities of the rumen microflora are therefore of crucial importance. But not all the bacteria are cellulolytic: many subsist on substrates (lactate, hydrogen) generated by other bacteria in the rumen.

The protozoa in the gut are also a complex mixture of specialists. Most are holotrich ciliates and entodinio-morphs. A few can digest cellulose. The cellulolytic ciliates have intrinsic cel-lulases, although some other protozoa may use bacterial symbionts. Some consume bacteria: in their absence the number of bacteria rise. Some of the entodiniomorphs prey on other protozoa. Thus, the diverse processes of competition, predation and mutualism, and the food chains that characterize terrestrial and aquatic communities in nature, are all present within the rumen microcosm.

a complex community of mutualists

13.5.3 Refection

Eating feces is a taboo amongst humans, presumably through some combination of biological and cultural evolution in response to the health hazards posed by pathogenic microbes, including many that are relatively harmless in the hindgut but are pathogenic in more anterior regions. For many vertebrates, however, symbiotic microbes, living in the hindgut beyond the regions where effective nutrient absorption is possible, are a resource that is too good to waste. Thus coprophagy (eating feces) or refection (eating one's own feces) is a regular practice in many small herbivorous mammals. This is developed to a fine art in species such as rabbits that have a 'colonic separation mechanism' that allows them to produce separate dry, non-nutritious fecal pellets and soft, more nutritious pellets that they consume selectively. These contain high levels of SCFAs, microbial protein and B vitamins, and can provide 30% of a rabbit's nitrogen requirements and more B vitamins than it requires (Bjornhag, 1994; Stevens & Hume, 1998).

13.5.4 Termite guts

Termites are social insects of the order Isoptera, many of which depend on mutualists for the digestion of wood. Primitive termites feed directly on wood, and most of the cellulose, hemicelluloses and possibly lignins are digested by mutualists in the gut (Figure 13.11), where the paunch (part of the segmented hindgut) forms a microbial fermentation chamber. However, the advanced termites (75% of all the species) rely much more heavily on their own cellulase (Hogan et al., 1988), while a third group (the Macrotermitinae) cultivate wood-digesting fungi that the termites eat along with the wood itself, which the fungal cellulases assist in digesting.

Termites refecate, so that food material passes at least twice through the gut, and microbes that have reproduced during the first passage may be digested the second time round. The major group of microorganisms in the paunch of primitive termites are anaerobic flagellate protozoans. Bacteria are also present, but cannot digest cellulose. The protozoa engulf particles of wood and ferment the cellulose within their cells, releasing carbon dioxide and hydrogen. The principal products, subsequently absorbed by the host, are SCFAs (as in vertebrates) but in termites they are primarily acetic acid.

The bacterial population of the termite gut is less conspicuous than that of the rumen, but appears to play a part in two distinct mutualisms.

Figure 13.11 Electron micrograph of a thin section of the paunch of the termite Reticulitermes flavipes. Much of the flora is composed of aggregates of bacteria. Amongst them can be seen endospore-forming bacteria (E), spirochetes (S) and protozoa. (After Breznak, 1975.)

Figure 13.11 Electron micrograph of a thin section of the paunch of the termite Reticulitermes flavipes. Much of the flora is composed of aggregates of bacteria. Amongst them can be seen endospore-forming bacteria (E), spirochetes (S) and protozoa. (After Breznak, 1975.)

Succinimonas Amylolytic

Figure 13.12 The phylogeny of selected aphids and their corresponding primary endosymbionts. Other bacteria are shown for comparison. The aphid phylogeny (after Heie, 1987) is shown on the left and the bacterial phylogeny on the right. Broken lines connect the associated aphids and bacteria. Three species of bacteria that are not endosymbionts are also shown in the phylogeny: Ec, Escherichia coli; Pv, Proteus vulgaris; Ra, Ruminobacter amylophilus (a rumen symbiont). The distances along the branches are drawn to be roughly proportionate to time. (After Moran et al., 1993.) Aphid species: Ap, Acyrthosiphon pisum; Cv, Chaitophorus viminalis; Dn, Diuraphis noxia; Mp, Myzus persicae; Mr, Melaphis rhois; Mv, Mindarus victoriae; Pb, Pemphigus betae; Rm, Rhopalosiphum maidis; Rp, Rhodalosiphon padi; Sc, Schlectendalia chinensis; Sg, Schizaphis graminum; Us, Uroleucon sonchi.

Aphid phylogeny

Asian

Melaphidina

48-70 Myr ago

American

80-160 Myr ago

80-120 Myr ago

30-80 Myr ago

Ra Pv Ec

Sc Mr Pb Mv Cv Dn

Bacterial phylogeny

Origin of endosymbiotic association

1 Spirochetes tend to be concentrated at the surface of the flagellates. The spirochetes possibly receive nutrients from the flagellates, and the flagellates gain mobility from the movements of the spirochetes: a pair of mutualists living mutualistically within a third species.

2 Some bacteria in the termite gut are capable of fixing gaseous nitrogen - apparently the only clearly established example of nitrogen-fixing symbionts in insects (Douglas, 1992). Nitrogen fixation stops when antibacterial antibiotics are eaten (Breznak, 1975), and the rate of nitrogen fixation falls off sharply if the nitrogen content of the diet is increased.

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