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

Abstract

Summary: 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: P ichia anomala , A cinetobacter spp. and P seudomonas putida ; specialists such as D unaliella salina , S accharomyces cerevisiae , L actobacillus spp. and other lactic acid bacteria; freshwater autotrophs G onyostomum semen and M icrocystis aeruginosa ; obligate anaerobes such as C lostridium acetobutylicum ; facultative pathogens such as R hodotorula mucilaginosa , P antoea ananatis and P seudomonas aeruginosa ; and other extremotolerant and extremophilic microbes such as A spergillus spp., S alinibacter ruber and H aloquadratum 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.