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Grand Challenges in Microbial Symbiosis Research SPECIALTY GRAND CHALLENGE ARTICLE published: 10 April 2014 doi: 10.3389/fmicb.2014.00164 Cooperation, communication, and co-evolution: grand challenges in microbial symbiosis research Nicole S. Webster* Australian Institute of Marine Science, Townsville, QLD, Australia *Correspondence: [email protected] Edited by: Martin G. Klotz, University of North Carolina at Charlotte, USA Reviewed by: Colleen Cavanaugh, Harvard University, USA Russell T. Hill, University of Maryland Center for Environmental Science, USA Keywords: symbiosis, microbe, host, challenge, holobiont, meta-organism, co-evolution Microorganisms form symbiotic partner- persistence and ultimately the survival of zooxanthellae which contribute photosyn- ships with eukaryotes that span all evo- their host (Horn et al., 2004). Microbial thates critical for growth and survival of lutionary stages, from simple amoebae parasitism has been (and is still) a pri- their coral hosts (Muscatine and Porter, through to humans. The term sym- mary focus of research into symbiotic 1977). Many of these examples involve biosis originates from the Greek word interactions largely due to the adverse only one, or relatively few, microbial sym- “Symbioun” meaning “to live together” impacts pathogens have on human health bionts and are therefore tractable models and was defined by Anton deBary in and the deleterious effects they have on for obtaining insights into host symbiont 1879 as “the living together of two dis- agricultural and animal stocks. However, ecology and evolution. Investigations of similar organisms, usually in intimate beneficial microbial infections whereby these low microbial diversity systems have association, and usually to the bene- hosts gain resources or services that greatly enhanced our understanding of fit of at least one partner” (De Bary, enhance their fitness are known to be mechanistic interactions, such as molec- 1879). Whilst the original deBary defi- just as ubiquitous as parasitic ones and are ular communication and co-metabolism, nition encompasses pathogens and com- rapidly gaining research traction. Research between the symbiotic partners (Dale and mensals, the term “microbial symbiont” on both parasitic and mutualistic associa- Moran, 2006). Novel evolutionary prin- is most commonly used to describe a tions provide insights into the mechanisms ciples such as genome reduction, which microorganism that forms a mutualism— of host-symbiont interactions, such as facilitates a transition of the symbiotic a specific, stable and beneficial associ- recognition / specificity adaptations etc., relationship from facultative to obligate, ation with its host (Nyholm and Graf, and challenges for the field of microbial have also been revealed by comparative 2012). Importantly, symbiotic members symbiosis research can therefore largely be genome analysis of single symbiont sys- are “partners” and whilst the term “host” considered independent of the nature of tems (Moran, 2002; Moran et al., 2008). may imply that one partner accommo- the interaction. However, microbial symbioses range dates or facilitates the association, both Symbiosis research has historically in complexity from those with a sin- members of microbial mutualisms actively focused on associations that (i) have eco- gle microorganism to those with many contribute to the relationship and the term nomic importance, e.g., nitrogen fixing hundreds or thousands of obligate or fac- “host” merely indicates the larger part- rhizobia in commercial legume species ultative symbionts, e.g., termite hindgut ner. This Grand Challenge Article briefly (Gage, 2004), (ii) have implications for (Hongoh, 2011), human gut (Marchesi, summarizes the current state of micro- human health, e.g., Helicobacter pylori 2010) and marine sponges (Webster and bial symbiosis research and identifies the which is responsible for duodenal and Taylor, 2012). The development of next methodological and conceptual challenges gastric ulcers in humans or (iii) offer generation sequencing (NGS) methods facing the field into the future. ecologically fascinating insights, e.g., has intensified research into these more Microbial symbioses are generally cat- Wolbachia that can significantly alter the complex microbial symbiont communi- egorized as parasitism, commensalism, reproductive capabilities of insect hosts ties, facilitating analysis of both diversity or mutualism, though some relation- (Serbus et al., 2008), bioluminescent vib- and functionality. ships may wander across these defined rio that occupy the light organ of bobtail The vast majority of microbial sym- boundaries depending on evolution- squid and provide luminescence for host bionts are not amenable to traditional ary processes, changes in environmental feeding and camouflage (McFall-Ngai, cultivation methods and the applica- conditions and/or health state of the 2008b), chemoautotrophic symbionts that tion of genetic and genomic approaches host/symbiont. These include cases such convert compounds like hydrogen sulfide has therefore dramatically accelerated as chlamydia where microbes initially and carbon dioxide into organic molecules research in the field of microbial sym- infect hosts as pathogens but over time on which their deep sea hydrothermal vent biosis (McFall-Ngai, 2008a). NGS projects have evolved mechanisms that assist their hosts can feed (Dubilier et al., 2008)and are producing an almost overwhelming www.frontiersin.org April 2014 | Volume 5 | Article 164 | 1 Webster Grand challenges in microbial symbiosis amount of data and this revolution in scolopes and its bioluminescent bacterial Symbionts can also be transmitted ver- delivery of molecular information has symbiont Vibrio fischeri is a classic exam- tically through reproductive cells and lar- fundamentally altered our understanding ple of “winnowing”- a gradual elimina- vae, as has been demonstrated in insects of microbial symbiosis. As an increas- tion of potential light organ colonizers (Moran and Baumann, 2000), ascidi- ing number of host-associated microbial that ensures separation of the specific ans (Kojima and Hirose, 2012), sponges environments are explored using NGS, strain of symbiotic V. fischer i from the (Usher et al., 2001; Webster et al., 2010) estimates of microbial diversity have milieu of environmental microbes present andadiverserangeofotherhigherorgan- exploded [e.g., a recent analysis of ascidian in the seawater (Nyholm and McFall-Ngai, isms (McFall-Ngai, 2002). In contrast to species documented 3217 unique bacterial 2004). The evolution of symbiont-specific the phylogenetically diverse communities OTU’S, (Erwin et al., 2014)], unexpected factors for colonization was also recently that can establish a symbiosis through hor- genomic features have been uncovered highlighted by analysis of Bacillus in the izontal acquisition, vertical transmission [e.g., extreme genome reduction has been mouse gut where novel molecular mecha- generally leads to more streamlined micro- reported in a wide range of bacterial sym- nisms in the symbiont were found to con- bial communities with reduced taxonomic bionts (McCutcheon and Moran, 2012)], trol the specificity and stability of other gut and functional complexity. A classic exam- functional equivalence and evolution- microbiota (Lee et al., 2013). ple of vertical transmission is the symbio- ary convergence has been reported in In terms of host acquisition, sym- sis between the pea aphid Acrythosiphon complex symbiont communities (Fan bionts can be acquired (i) horizontally pisum and its nutritional endosymbiont et al., 2012) and unexpected patterns from the environment, e.g., from food Buchnera aphidicola. This symbiosis was of host-specificity have been revealed in the human gut (Ley et al., 2008)or established over 160 million years ago [e.g., previously considered sponge— contemporaries, e.g., “egg smearing,” in and is maintained through strict verti- specific bacterial sequences have now stinkbugs which involves the female con- cal transmission (Baumann, 2005). The been recovered from the rare biosphere taminating the surface of her eggs with endosymbionts are contained within bac- of diverse marine environments (Taylor symbiont-laden feces during oviposition teriocytes in a region of the aphid body et al., 2013)]. These studies herald an era (reviewed in Funkhouser and Bordenstein, cavity that allows their successful transfer of unprecedented discovery in symbio- 2013), (ii) vertically from parental inher- to developing oocytes or embryos dur- sis research yet also reveal the daunting itance or (iii) via a combination of ing aphid reproduction (Baumann et al., scale of the task ahead in deciphering the these mechanisms (Bright and Bulgheresi, 1995). This mutualism is so obligate that forces that drive relationships within these 2010). Horizontal symbiont transmission neither the host nor the symbiont can complex symbiotic systems. often leads to selection based on sym- reproduce independently. Genome anal- Lifestyles of bacterial symbionts can biont function rather than symbiont tax- ysis of the symbiont revealed genes for vary in four important ways, all of which onomy (Turnbaugh and Gordon, 2009; biosyntheses of amino acids required by contribute to the long term evolution of Burke et al., 2011). Establishing horizon- the host and an absence of non-essential symbiotic microbial lineages as well as the tally acquired symbioses presents consid- amino acids, indicating complementarity co-evolution of the holobiont: (1) host- erable challenges for both the host and and
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