Interspecies interactions within oral microbial communities

Abstract

While reductionism has greatly advanced microbiology in the past 400 years, assembly of smaller pieces just could not explain the whole! Modern microbiologists are learning "system thinking" and "holism." Such an approach is changing our understanding of microbial physiology and our ability to diagnose/treat microbial infections. This review uses oral microbial communities as a focal point to describe this new trend. With the common name "dental plaque," oral microbial communities are some of the most complex microbial floras in the human body, consisting of more than 700 different bacterial species. For a very long time, oral microbiologists endeavored to use reductionism to identify the key genes or key pathogens responsible for oral microbial pathogenesis. The limitations of reductionism forced scientists to begin adopting new strategies using emerging concepts such as interspecies interaction, microbial community, biofilms, polymicrobial disease, etc. These new research directions indicate that the whole is much more than the simple sum of its parts, since the interactions between different parts resulted in many new physiological functions which cannot be observed with individual components. This review describes some of these interesting interspecies-interaction scenarios.

FIG. 1.

Evolution of microbiological studies. Initial reductionism included zooming in from complex multispecies microbial communities to isolated genes from individual species. This process was followed by an expansion of scope based on the knowledge acquired through reductionism to achieve a holistic view of the interactions of different bacterial species and the multispecies communities in which they reside.

FIG. 2.

Oral bacteria observed by Anton van Leeuwenhoek and their contemporary equivalents. (a) The original drawings by van Leeuwenhoek. The bacterium designated A was later suggested to be a rod-shaped motile bacterium such as Campylobacter rectus (b) (photo courtesy: National Research Council Canada); the highly motile species shown in his original drawing as B and moving quickly from C to D was likely Selenomonas sputigena (c) (electron micrograph, modified from reference with permission) (187), whereas E was proposed to be oral cocci (d) (atomic force microscopy image). van Leeuwenhoek's original drawing G was disputed as being either a Spirillum sp. (not shown) or an oral spirochete such as Treponema denticola (e) (electron micrograph), and the long fusiform species designated F were proposed to be Leptotrichia (Leptotrix) buccalis (f) (electron micrograph, modified from reference with permission).

FIG. 3.

Illustration of interspecies interactions between Streptococcus mutans and selected oral streptococci that have been studied on a molecular level. (a) Interactions of S. mutans with S. gordonii, S. oligofermentans, and S. sanguinis. Depicted is the production of lactic acid, mutacin, and CSP, which also enhances mutacin production by S. mutans. Lactic acid has been found to inhibit proliferation of a variety of acid-sensitive anaerobe species, but it was recently discovered to serve as a substrate for S. oligofermentans for H₂O₂ production. This compound is also generated by S. sanguinis and was previously shown to inhibit growth of S. mutans. S. sanguinis and S. gordonii are sensitive to the mutacins produced by S. mutans. In contrast to S. sanguinis, which can inhibit S. mutans by its ability to produce H₂O₂, S. gordonii utilizes challisin to reduce mutacin production by reducing the levels of the stimulating factor CSP. The dashed arrow in combination with + indicates stimulation, solid arrows symbolize production, and ⊣ in combination with − designates inhibition. The shaded area indicates the timing-sensitive interactions between S. mutans and S. sanguinis illustrated in panel b. (b) Importance of timing for reciprocal inhibition of S. mutans (Sm) and S. sanguinis (Ss). Given a 1-day growth advantage, S. mutans inhibits S. sanguinis via its mutacin production (upper panel), whereas S. sanguinis controls establishment of S. mutans by its ability to generate H₂O₂ when given the same 1-day advantage (middle panel). Without the benefit to either of establishing itself earlier, both species coexist without any apparent mutual inhibition (lower panel). For further details, see the text.