Chemosynthetic symbioses between bacteria and marine invertebrates were discovered 30 years ago at hydrothermal vents on the Galapagos Rift. Remarkably, it took the discovery of these symbioses in the deep sea for scientists to realize that chemosynthetic symbioses occur worldwide in a wide range of habitats, including cold seeps, whale and wood falls, shallow-water coastal sediments and continental margins. The evolutionary success of these symbioses is evident from the wide range of animal groups that have established associations with chemosynthetic bacteria; at least seven animal phyla are known to host these symbionts. The diversity of the bacterial symbionts is equally high, and phylogenetic analyses have shown that these associations have evolved on multiple occasions by convergent evolution. This Review focuses on the diversity of chemosynthetic symbionts and their hosts, and examines the traits that have resulted in their evolutionary success.
Symbioses between bacteria and eukaryotes are ubiquitous, yet our understanding of the interactions driving these associations is hampered by our inability to cultivate most host-associated microbes. Here, we used a metagenomic approach to describe four co-occurring symbionts from the marine oligochaete Olavius algarvensis, a worm lacking a mouth, gut, and nephridia. Shotgun sequencing and metabolic pathway reconstruction revealed that the symbionts are sulfur-oxidizing and sulfate-reducing bacteria, all of which are capable of carbon fixation, providing the host with multiple sources of nutrition. Molecular evidence for the uptake and recycling of worm waste products by the symbionts suggests how the worm could eliminate its excretory system, an adaptation unique among annelid worms. We propose a model which describes how the versatile metabolism within this symbiotic consortium provides the host with an optimal energy supply as it shuttles between the upper oxic and lower anoxic coastal sediments which it inhabits. 3 Symbiosis plays a major role in shaping the evolution and diversity of eukaryotic organisms 1 . Remarkably, only recently has there been an emerging recognition that most eukaryotic organisms are intimately associated with a complex community of beneficial microbes that are essential for their development, health, and interactions with the environment 2 . This renaissance in symbiosis research stems from advances in molecular approaches that have enabled the study of natural microbial consortia using cultivationindependent methods [3][4][5] . Metagenomic analyses have provided a new dimension in the study of community organization and metabolism in natural microbial communities [6][7][8][9][10] .To date, however, genomic analyses of symbiotic microbes from eukaryotes have been confined to individual strains (for the only exception see Wu et al. 11), limiting our ability to understand the intricate interactions involving communication, competition, and resource partitioning that shape symbiotic microbial communities.Here, we used random shotgun sequencing and nucleotide-signature based binning to study the symbiotic community in Olavius algarvensis. This marine worm belongs to a group of oligochaetes (phylum Annelida) that lack a mouth, gut, and anus, and are unique among annelid worms in having reduced their nephridial excretory system 12 . They live in obligate and species-specific associations with multiple extracellular bacterial endosymbionts located just below the worm cuticle 12 . Since the symbionts have yet to be grown in culture, their phylogeny has only been accessible through 16S rRNA analysis and fluorescence in situ hybridization (FISH) 13,14 . O. algarvensis lives in coastalMediterranean sediments and harbors a chemoautotrophic sulfur-oxidizing Gammaproteobacterium ( 1 symbiont) and a deltaproteobacterial sulfate reducer ( 1 symbiont), recently shown to be engaged in an endosymbiotic sulfur cycle 14. An additional gamma-and deltaproteobacterial symbiont ( 3 and 4 symbionts) of ...
Termites effectively feed on many types of lignocellulose assisted by their gut microbial symbionts. To better understand the microbial decomposition of biomass with varied chemical profiles, it is important to determine whether termites harbor different microbial symbionts with specialized functionalities geared toward different feeding regimens. In this study, we compared the microbiota in the hindgut paunch of Amitermes wheeleri collected from cow dung and Nasutitermes corniger feeding on sound wood by 16S rRNA pyrotag, comparative metagenomic and metatranscriptomic analyses. We found that Firmicutes and Spirochaetes were the most abundant phyla in A. wheeleri, in contrast to N. corniger where Spirochaetes and Fibrobacteres dominated. Despite this community divergence, a convergence was observed for functions essential to termite biology including hydrolytic enzymes, homoacetogenesis and cell motility and chemotaxis. Overrepresented functions in A. wheeleri relative to N. corniger microbiota included hemicellulose breakdown and fixed-nitrogen utilization. By contrast, glycoside hydrolases attacking celluloses and nitrogen fixation genes were overrepresented in N. corniger microbiota. These observations are consistent with dietary differences in carbohydrate composition and nutrient contents, but may also reflect the phylogenetic difference between the hosts.
Bathymodiolus azoricus and Bathymodiolus puteoserpentis are symbiont-bearing mussels that dominate hydrothermal vent sites along the northern Mid-Atlantic Ridge (MAR). Both species live in symbiosis with two physiologically and phylogenetically distinct Gammaproteobacteria: a sulfur-oxidizing chemoautotroph and a methane-oxidizer. A detailed analysis of mussels collected from four MAR vent sites (Menez Gwen, Lucky Strike, Rainbow, and Logatchev) using comparative 16S rRNA sequence analysis and fluorescence in situ hybridization (FISH) showed that the two mussel species share highly similar to identical symbiont phylotypes. FISH observations of symbiont distribution and relative abundances showed no obvious differences between the two host species. In contrast, distinct differences in relative symbiont abundances were observed between mussels from different sites, indicating that vent chemistry may influence the relative abundance of thiotrophs and methanotrophs in these dual symbioses.
BackgroundProkaryotes dominate the biosphere and regulate biogeochemical processes essential to all life. Yet, our knowledge about their biology is for the most part limited to the minority that has been successfully cultured. Molecular techniques now allow for obtaining genome sequences of uncultivated prokaryotic taxa, facilitating in-depth analyses that may ultimately improve our understanding of these key organisms.ResultsWe compared results from two culture-independent strategies for recovering bacterial genomes: single-amplified genomes and metagenome-assembled genomes. Single-amplified genomes were obtained from samples collected at an offshore station in the Baltic Sea Proper and compared to previously obtained metagenome-assembled genomes from a time series at the same station. Among 16 single-amplified genomes analyzed, seven were found to match metagenome-assembled genomes, affiliated with a diverse set of taxa. Notably, genome pairs between the two approaches were nearly identical (average 99.51% sequence identity; range 98.77–99.84%) across overlapping regions (30–80% of each genome). Within matching pairs, the single-amplified genomes were consistently smaller and less complete, whereas the genetic functional profiles were maintained. For the metagenome-assembled genomes, only on average 3.6% of the bases were estimated to be missing from the genomes due to wrongly binned contigs.ConclusionsThe strong agreement between the single-amplified and metagenome-assembled genomes emphasizes that both methods generate accurate genome information from uncultivated bacteria. Importantly, this implies that the research questions and the available resources are allowed to determine the selection of genomics approach for microbiome studies.Electronic supplementary materialThe online version of this article (10.1186/s40168-018-0550-0) contains supplementary material, which is available to authorized users.
The advent of novel sequencing techniques has unraveled a tremendous diversity on Earth. Genomic data allow us to understand ecology and function of organisms that we would not otherwise know existed. However, major methodological challenges remain, in particular for multicellular organisms with large genomes. Arbuscular mycorrhizal (AM) fungi are important plant symbionts with cryptic and complex multicellular life cycles, thus representing a suitable model system for method development. Here, we report a novel method for large scale, unbiased nuclear sorting, sequencing, and de novo assembling of AM fungal genomes. After comparative analyses of three assembly workflows we discuss how sequence data from single nuclei can best be used for different downstream analyses such as phylogenomics and comparative genomics of single nuclei. Based on analysis of completeness, we conclude that comprehensive de novo genome assemblies can be produced from six to seven nuclei. The method is highly applicable for a broad range of taxa, and will greatly improve our ability to study multicellular eukaryotes with complex life cycles.
Morphological characters and nuclear ribosomal DNA (rDNA) phylogenies have so far been the basis of the current classifications of arbuscular mycorrhizal (AM) fungi. Improved understanding of the evolutionary history of AM fungi requires extensive ortholog sampling and analyses of genome and transcriptome data from a wide range of taxa. To circumvent the need for axenic culturing of AM fungi we gathered and combined genomic data from single nuclei to generate de novo genome assemblies covering seven families of AM fungi. We successfully sequenced the genomes of 15 AM fungal species for which genome data was not previously available. Comparative analysis of the previously published Rhizophagus irregularis DAOM197198 assembly confirm that our novel workflow generates genome assemblies suitable for phylogenomic analysis. Predicted genes of our assemblies, together with published protein sequences of AM fungi and their sister clades, were used for phylogenomic analyses. We evaluated the phylogenetic placement of Glomeromycota in relation to its sister phyla (Mucoromycota and Mortierellomycota), and found no support to reject a polytomy. Finally, we explored the phylogenetic relationships within Glomeromycota. Our results support family level classification from previous phylogenetic studies, and the polyphyly of the order Glomerales with Claroideoglomeraceae as the sister group to Glomeraceae and Diversisporales.
Gutless phallodrilines are marine annelid worms without a mouth or gut, which live in an obligate association with multiple bacterial endosymbionts that supply them with nutrition. In this study, we discovered an unusual symbiont community in the gutless phallodriline Inanidrilus exumae that differs markedly from the microbiomes of all 22 of the other host species examined. Comparative 16S rRNA gene sequence analysis and fluorescence in situ hybridization revealed that I. exumae harbors cooccurring gamma-, alpha-, and deltaproteobacterial symbionts, while all other known host species harbor gamma- and either alpha- or deltaproteobacterial symbionts. Surprisingly, the primary chemoautotrophic sulfur oxidizer “Candidatus Thiosymbion” that occurs in all other gutless phallodriline hosts does not appear to be present in I. exumae. Instead, I. exumae harbors a bacterial endosymbiont that resembles “Ca. Thiosymbion” morphologically and metabolically but originates from a novel lineage within the class Gammaproteobacteria. This endosymbiont, named Gamma 4 symbiont here, had a 16S rRNA gene sequence that differed by at least 7% from those of other free-living and symbiotic bacteria and by 10% from that of “Ca. Thiosymbion.” Sulfur globules in the Gamma 4 symbiont cells, as well as the presence of genes characteristic for autotrophy (cbbL) and sulfur oxidation (aprA), indicate that this symbiont is a chemoautotrophic sulfur oxidizer. Our results suggest that a novel lineage of free-living bacteria was able to establish a stable and specific association with I. exumae and appears to have displaced the “Ca. Thiosymbion” symbionts originally associated with these hosts.IMPORTANCE All 22 gutless marine phallodriline species examined to date live in a highly specific association with endosymbiotic, chemoautotrophic sulfur oxidizers called “Ca. Thiosymbion.” These symbionts evolved from a single common ancestor and represent the ancestral trait for this host group. They are transmitted vertically and assumed to be in transition to becoming obligate endosymbionts. It is therefore surprising that despite this ancient, evolutionary relationship between phallodriline hosts and “Ca. Thiosymbion,” these symbionts are apparently no longer present in Inanidrilus exumae. They appear to have been displaced by a novel lineage of sulfur-oxidizing bacteria only very distantly related to “Ca. Thiosymbion.” Thus, this study highlights the remarkable plasticity of both animals and bacteria in establishing beneficial associations: the phallodriline hosts were able to acquire and maintain symbionts from two very different lineages of bacteria, while sulfur-oxidizing bacteria from two very distantly related lineages were able to independently establish symbiotic relationships with phallodriline hosts.
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