First detection of thiotrophic symbiont phylotypes in the pelagic marine environment

Heindl, Niels R.; Gruber‐Vodicka, Harald R.; Bayer, Christoph; Lücker, Sebastian; Ott, Jörg; Bulgheresi, Silvia

doi:10.1111/j.1574-6941.2011.01096.x

Cited by 15 publications

(17 citation statements)

References 27 publications

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“…The other sequences were found in surface waters close to sediments containing stilbonematines and gutless phallodrilines, but could only be amplified using the highly sensitive, and contamination‐prone nested PCR approach (Heindl et al . ).…”

Section: Discussionmentioning

confidence: 97%

“…), and (ii) the amplification of partial 16S rRNA gene sequences with high similarity to symbiont sequences of stilbonematine nematodes from surface seawaters (Heindl et al . ) (but see below under ‘Repeated host switches between animal phyla’ for a more detailed discussion of environmental sequences closely related to stilbonematine ectosymbionts). Convincing evidence for codivergence in symbioses with horizontal acquisition is, however, rare (Bright & Bulgheresi ).…”

Section: Discussionmentioning

confidence: 99%

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Closely coupled evolutionary history of ecto‐ and endosymbionts from two distantly related animal phyla

et al. 2016

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The level of integration between associated partners can range from ectosymbioses to extracellular and intracellular endosymbioses, and this range has been assumed to reflect a continuum from less intimate to evolutionarily highly stable associations. In this study, we examined the specificity and evolutionary history of marine symbioses in a group of closely related sulphur-oxidizing bacteria, called Candidatus Thiosymbion, that have established ecto-and endosymbioses with two distantly related animal phyla, Nematoda and Annelida. Intriguingly, in the ectosymbiotic associations of stilbonematine nematodes, we observed a high degree of congruence between symbiont and host phylogenies, based on their ribosomal RNA (rRNA) genes. In contrast, for the endosymbioses of gutless phallodriline annelids (oligochaetes), we found only a weak congruence between symbiont and host phylogenies, based on analyses of symbiont 16S rRNA genes and six host genetic markers. The much higher degree of congruence between nematodes and their ectosymbionts compared to those of annelids and their endosymbionts was confirmed by cophylogenetic analyses. These revealed 15 significant codivergence events between stilbonematine nematodes and their ectosymbionts, but only one event between gutless phallodrilines and their endosymbionts. Phylogenetic analyses of 16S rRNA gene sequences from 50 Cand. Thiosymbion species revealed seven well-supported clades that contained both stilbonematine ectosymbionts and phallodriline endosymbionts. This closely coupled evolutionary history of marine ecto-and endosymbionts suggests that switches between symbiotic lifestyles and between the two host phyla occurred multiple times during the evolution of the Cand. Thiosymbion clade, and highlights the remarkable flexibility of these symbiotic bacteria.

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Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 99%

Closely coupled evolutionary history of ecto‐ and endosymbionts from two distantly related animal phyla

et al. 2016

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“…Both thiotrophy and symbiosis have repeatedly evolved in basal Gammaproteobacteria [1] and many clades of thiotrophic symbionts are either affiliated with more than one clade of host organisms, or have free-living members [17,49,50]. The Ca .…”

Section: Discussionmentioning

confidence: 99%

Specificity in diversity: single origin of a widespread ciliate-bacteria symbiosis

et al. 2017

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Symbioses between eukaryotes and sulfur-oxidizing (thiotrophic) bacteria have convergently evolved multiple times. Although well described in at least eight classes of metazoan animals, almost nothing is known about the evolution of thiotrophic symbioses in microbial eukaryotes (protists). In this study, we characterized the symbioses between mouthless marine ciliates of the genus Kentrophoros, and their thiotrophic bacteria, using comparative sequence analysis and fluorescence in situ hybridization. Ciliate small-subunit rRNA sequences were obtained from 17 morphospecies collected in the Mediterranean and Caribbean, and symbiont sequences from 13 of these morphospecies. We discovered a new Kentrophoros morphotype where the symbiont-bearing surface is folded into pouch-like compartments, illustrating the variability of the basic body plan. Phylogenetic analyses revealed that all investigated Kentrophoros belonged to a single clade, despite the remarkable morphological diversity of these hosts. The symbionts were also monophyletic and belonged to a new clade within the Gammaproteobacteria, with no known cultured representatives. Each host morphospecies had a distinct symbiont phylotype, and statistical analyses revealed significant support for host–symbiont codiversification. Given that these symbioses were collected from two widely separated oceans, our results indicate that symbiotic associations in unicellular hosts can be highly specific and stable over long periods of evolutionary time.

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“…Ecological studies performed in the 90s suggest that stilbonematids trophically depend on their ectosymbionts, and these, in turn, profit from nematode migrations through the sulfide gradient in the marine sediment (Ott et al 1991). All the molecularly identified ectosymbionts belong indeed to the marine oligochaete and nematode thiotrophic symbiont (MONTS) cluster, which comprises 16S rRNA-gene sequences retrieved from gammaproteobacterial sulfur oxidizers associated with these invertebrates, as well as sequences of environmental origin (Polz et al 1994;Bayer et al 2009;Bulgheresi et al 2011;Heindl et al 2011;Pende et al 2014). The closest cultivable relatives of MONTS members are free-living purple sulfur bacteria (Chromatiaceae).…”

Section: Why Dressing Up?mentioning

confidence: 99%

All the microbiology nematodes can teach us

Bulgheresi

2017

FEMS Microbiology Ecology

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One sentence summary: Nematode-bacterium associations are major research subjects. Complementing genetic studies with ecological ones is necessary to boost our understanding of how microbial symbioses evolved and how they impact the environment. Editor: Gerard Muyzer ABSTRACTBe it their pervasiveness, experimental tractability or their impact on human health and agriculture, nematode-bacterium associations are far-reaching research subjects. Although the omics hype did not spare them and helped reveal mechanisms of communication and exchange between the associated partners, a huge amount of knowledge still awaits to be harvested from their study. Here, I summarize and compare the kind of research that has been already performed on the model nematode Caenorhabditis elegans and on symbiotic nematodes, both marine and entomopathogenic ones. The emerging picture highlights how complementing genetic studies with ecological ones (in the case of well-established genetic model systems such as C. elegans) and vice versa (in the case of the yet uncultured Stilbonematinae) will deepen our understanding of how microbial symbioses evolved and how they impact our environment.

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First detection of thiotrophic symbiont phylotypes in the pelagic marine environment

Cited by 15 publications

References 27 publications

Closely coupled evolutionary history of ecto‐ and endosymbionts from two distantly related animal phyla

Closely coupled evolutionary history of ecto‐ and endosymbionts from two distantly related animal phyla

Specificity in diversity: single origin of a widespread ciliate-bacteria symbiosis

All the microbiology nematodes can teach us

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