The biology of habitat dominance; can microbes behave as weeds?

Abstract

Competition between microbial species is a product of, yet can lead to a reduction in, the microbial diversity of specific habitats. Microbial habitats can resemble ecological battlefields where microbial cells struggle to dominate and/or annihilate each other and we explore the hypothesis that (like plant weeds) some microbes are genetically hard-wired to behave in a vigorous and ecologically aggressive manner. These 'microbial weeds' are able to dominate the communities that develop in fertile but uncolonized--or at least partially vacant--habitats via traits enabling them to out-grow competitors; robust tolerances to habitat-relevant stress parameters and highly efficient energy-generation systems; avoidance of or resistance to viral infection, predation and grazers; potent antimicrobial systems; and exceptional abilities to sequester and store resources. In addition, those associated with nutritionally complex habitats are extraordinarily versatile in their utilization of diverse substrates. Weed species typically deploy multiple types of antimicrobial including toxins; volatile organic compounds that act as either hydrophobic or highly chaotropic stressors; biosurfactants; organic acids; and moderately chaotropic solutes that are produced in bulk quantities (e.g. acetone, ethanol). Whereas ability to dominate communities is habitat-specific we suggest that some microbial species are archetypal weeds including generalists such as: Pichia anomala, Acinetobacter spp. and Pseudomonas putida; specialists such as Dunaliella salina, Saccharomyces cerevisiae, Lactobacillus spp. and other lactic acid bacteria; freshwater autotrophs Gonyostomum semen and Microcystis aeruginosa; obligate anaerobes such as Clostridium acetobutylicum; facultative pathogens such as Rhodotorula mucilaginosa, Pantoea ananatis and Pseudomonas aeruginosa; and other extremotolerant and extremophilic microbes such as Aspergillus spp., Salinibacter ruber and Haloquadratum walsbyi. Some microbes, such as Escherichia coli, Mycobacterium smegmatis and Pseudoxylaria spp., exhibit characteristics of both weed and non-weed species. We propose that the concept of nonweeds represents a 'dustbin' group that includes species such as Synodropsis spp., Polypaecilum pisce, Metschnikowia orientalis, Salmonella spp., and Caulobacter crescentus. We show that microbial weeds are conceptually distinct from plant weeds, microbial copiotrophs, r-strategists, and other ecophysiological groups of microorganism. Microbial weed species are unlikely to emerge from stationary-phase or other types of closed communities; it is open habitats that select for weed phenotypes. Specific characteristics that are common to diverse types of open habitat are identified, and implications of weed biology and open-habitat ecology are discussed in the context of further studies needed in the fields of environmental and applied microbiology.

Figure 1

Percentage species composition during olive fermentations at (i) 2 days, (ii) 17 days and (iii) 35 days over a range of conditions: (A) with added NaCl (6% w/v); (B) added NaCl and glucose (6% and 0.5% w/v respectively); (C) added NaCl and lactic acid (6% w/v and 0.2% v/v respectively); and (D) NaCl, glucose and lactic acid (6% and 0.5% w/v, and 0.2% v/v respectively). Data (from Nisiotou et al., 2010) were obtained by DGGE.

Figure 2

Growth of Saccharomyces cerevisiae strains: (A) CCY-21-4-13, (B) Alcotec 8 and (C) CBS 6412 and other yeast species: (D) Candida etchellsii (UWOPS 01–168.3), (E) Cryptococcus terreus (PB4), (F) Debaryomyces hansenii (UWOPS 05-230.3), (G) Hansenula (Ogataea) polymorpha (CBS 4732), (H) Hortaea werneckii (MZKI B736), (I) Kluyveromyces marxianus (CBS 712), (J) Pichia (Kodamaea) ohmeri (UWOPS 05-228.2), (K) Pichia (Komagataella) pastoris (CBS 704), (L) Pichia sydowiorum (UWOPS 03-414.2), (M) Rhodotorula creatinivora (PB7), (N) Saccharomycodes ludwigii (UWOPS 92–218.4) and (O) Zygosaccharomyces rouxii (CBS 732) on a range of media at 30°C. These were: malt-extract, yeast-extract phosphate agar (MYPiA) without added solutes (control), and MYPiA supplemented with diverse stressors – ethanol, methanol, glycerol, fructose, sucrose, NaCl, MgCl₂, ammonium sulfate, proline, xantham gum and polyethylene glycol (PEG) 8000 – over a range of concentrations as shown in key (values indicate %, w/v). A standard Spot Test was carried out (see Chin et al., ; Toh et al., 2001) that was modified from Albertyn and colleagues (1994) for stress phenotype characterization (see Table 5). Colony density was assessed after an incubation time of 24 h on a scale of 0–5 arbitrary units (Chin et al., 2010). Cultures were obtained from (for strain A) the Culture Collection of Yeasts (CCY, Slovakia); (strain B) Hambleton Bard Ltd, Chesterfield, UK; (strains C, G, I, K, O) the Centraalbureau voor Schimmelcultures (CBS, the Netherlands); (strains D, F, J, L, N) the University of Western Ontario Plant Sciences Culture Collection (UWOPS, Canada); (strains E, M) were obtained from Dr Rosa Margesin, Institute of Microbiology, Leopold Franzens University, Austria; and (strain H) the Microbial Culture Collection of National Institute of Chemistry (MZKI, Slovenia). All Petri plates containing the same medium were sealed in a polythene bag to maintain water; all experiments were carried out in duplicate, and plotted values are the means of independent treatments.