'Til death do us part': Coming to terms with symbiotic relationships

Stanford University, and VA Palo Alto Health Care System, Building 101, Room B4-185, 3801 Miranda Avenue 154T, Palo Alto, California 94304, USA.
Nature Reviews Microbiology (Impact Factor: 23.57). 11/2008; 6(10):721-4. DOI: 10.1038/nrmicro1990
Source: PubMed


Symbiotic interactions of microorganisms are widespread in nature, and support fundamentally important processes in diverse areas of biology that range from health and disease to ecology and the environment. Here, David Relman discusses the selection of articles in this Focus issue, which reflects the exciting advances in our understanding of intimate partnerships between organisms and their environments.

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    • "Many of the documented relationships are complicated and understudied, and involve multipartite symbioses. Multipartite symbioses are the beneficial , harmful, and neutral relationships that can change over time among multiple organisms (adapted from Relman, 2008). The nematodes associated with bark beetles can be endoparasites (transported internally) or ectoparasites (transported externally on the body surface or transported in nematangia, specialized pocket-like structures on the jugal wing folds of the bark beetles (Cardoza et al., 2008). "
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    ABSTRACT: Symbiotic interactions are prevalent in all bark beetle communities. For many species, the ability to associate with multiple partners enables species to persist through fluctuations in climate, resources, predation, and partner availability. Symbionts, particularly mutualistic species associated with bark beetles, can increase bark beetle fitness by providing nutrition or protection, exhaust or detoxify tree defenses, enhance communication, and promote or discourage other organisms. Alternatively, symbiotic species that are antagonistic to bark beetles can negatively affect bark beetle fitness directly (e.g., pathogens of bark beetles) or indirectly (e.g., competing with mutualistic microbes within trees). Symbionts associated with bark beetles have also been used to better understand the basic field of science such as mutualism theory, evolutionary and ecology adaption (e.g., horizontal gene transfer), and drivers of population dynamics. In general, bark beetle symbionts are known to affect mechanisms of evolution, coadaptation and speciation, tree defenses, chemical communication, population dynamics, range expansion, and pest management. Symbionts can have multiple roles, and interactions can change as species and environments change. Thus, simply categorizing symbionts as mutualistic, antagonistic, commensal etc. can be misleading. The combinations of genomic, behavioral, and ecological research approaches that incorporate symbionts will help us better understand how symbionts affect bark beetles. These interactions and effects will be discussed in more detail in this chapter.
    Full-text · Chapter · Jan 2015
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    • "Bacteria living within the body or cells of eukaryotes are extremely abundant and widespread (Dale and Moran, 2006; Ryan et al., 2008; Kikuchi, 2009). These endosymbiotic bacteria often contribute to diverse metabolic host functions, making their presence favorable or even essential (Relman, 2008). Eventually, both the bacterial partner and the host may lose their autonomy and become strictly dependent on each other, resulting in an obligate association (Dale and Moran, 2006; Toft and Andersson, 2010). "
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    ABSTRACT: The siphonous green seaweed Bryopsis harbors complex intracellular bacterial communities. Previous studies demonstrated that certain species form close, obligate associations with Flavobacteriaceae. A predominant imprint of host evolutionary history on the presence of these bacteria suggests a highly specialized association. In this study we elaborate on previous results by expanding the taxon sampling and testing for host-symbiont coevolution Therefore, we optimized a PCR protocol to directly and specifically amplify Flavobacteriaceae endosymbiont 16S rRNA gene sequences, which allowed us to screen a large number of algal samples without the need for cultivation or surface sterilization. We analyzed 146 Bryopsis samples, and 92 additional samples belonging to the Bryopsidales and other orders within the class Ulvophyceae. Results indicate that the Flavobacteriaceae endosymbionts are restricted to Bryopsis, and only occur within specific, warm-temperate and tropical clades of the genus. Statistical analyses (AMOVA) demonstrate a significant non-random host-symbiont association. Comparison of bacterial 16S rRNA and Bryopsis rbcL phylogenies, however, reveal complex host-symbiont evolutionary associations, whereby closely related hosts predominantly harbor genetically similar endosymbionts. Bacterial genotypes are rarely confined to a single Bryopsis species and most Bryopsis species harbored several Flavobacteriaceae, obscuring a clear pattern of coevolution.
    Full-text · Article · Mar 2013 · Molecular Phylogenetics and Evolution
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    • "The relative contribution of these two processes could help determine the cost/benefit balance of an interaction, for example tipping a relationship over evolutionary time from a parasitic to a mutualistic one or vice versa. It is now well recognized that negative and beneficial interactions share many of the same host-microbe signalling pathways and cellular responses, including host innate immune responses to invading microbes (Hentschel et al., 2000; Relman, 2008; Schwarz, 2008). One tolerance-promoting (tolerogenic) mechanism employed by some parasites and pathogens of vertebrates involves modulation of the TGFb pathway during invasion (Ndungu et al., 2005; Simmons et al., 2006; Waghabi et al., 2005). "
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    ABSTRACT: Animals must manage interactions with beneficial as well as detrimental microbes. Immunity therefore includes strategies for both resistance to and tolerance of microbial invaders. Transforming growth factor beta (TGFβ) cytokines have many functions in animals including a tolerance-promoting (tolerogenic) role in immunity in vertebrates. TGFβ pathways are present in basal metazoans such as cnidarians but their potential role in immunity has never been explored. This study takes a two-part approach to examining an immune function for TGFβ in cnidarians. First bioinformatic analyses of the model anemone Aiptasia pallida were used to identify TGFβ pathway components and explore the hypothesis that an immune function for TGFβs existed prior to the evolution of vertebrates. A TGFβ ligand from A. pallida was identified as one that groups closely with vertebrate TGFβs that have an immune function. Second, cellular analyses of A. pallida were used to examine a role for a TGFβ pathway in the regulation of cnidarian-dinoflagellate mutualisms. These interactions are stable under ambient conditions but collapse under elevated temperature, a phenomenon called cnidarian bleaching. Addition of exogenous human TGFβ suppressed an immune response measured as LPS-induced nitric oxide (NO) production by the host. Addition of anti-TGFβ to block a putative TGFβ pathway resulted in immune stimulation and a failure of the symbionts to successfully colonize the host. Finally, addition of exogenous TGFβ suppressed immune stimulation in heat-stressed animals and partially abolished a bleaching response. These findings suggest that the dinoflagellate symbionts somehow promote host tolerance through activation of tolerogenic host immune pathways, a strategy employed by some intracellular protozoan parasites during their invasion of vertebrates. Insight into the ancient, conserved nature of host-microbe interactions gained from this cnidarian-dinoflagellate model is valuable to understanding the evolution of immunity and its role in the regulation of both beneficial and detrimental associations.
    Full-text · Article · Sep 2012 · Developmental and comparative immunology
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