Bacteriophage flux in endosymbionts (Wolbachia): infection frequency, lateral transfer, and recombination rates

The highly specialized genomes of bacterial endosymbionts typically lack one of the major contributors of genomic flux in the free-living microbial world-bacteriophages. This study yields three results that show bacteriophages have, to the contrary, been influential in the genome evolution of the most prevalent bacterial endosymbiont of invertebrates, Wolbachia. First, we show that bacteriophage WO is more widespread in Wolbachia than previously recognized, occurring in at least 89% (35/39) of the sampled genomes. Second, we show through several phylogenetic approaches that bacteriophage WO underwent recent lateral transfers between Wolbachia bacteria that coinfect host cells in the dipteran Drosophila simulans and the hymenopteran Nasonia vitripennis. These two cases, along with a previous report in the lepidopteran Ephestia cautella, support a general mechanism for genetic exchange in endosymbionts--the "intracellular arena" hypothesis--in which genetic material moves horizontally between bacteria that coinfect the same intracellular environment. Third, we show recombination in this bacteriophage; in the region encoding a putative capsid protein, the recombination rate is faster than that of any known recombining genes in the endosymbiont genome. The combination of these three lines of genetic evidence indicates that this bacteriophage is a widespread source of genomic instability in the intracellular bacterium Wolbachia and potentially the invertebrate host. More generally, it is the first bacteriophage implicated in frequent lateral transfer between the genomes of bacterial endosymbionts. Gene transfer by bacteriophages could drive significant evolutionary change in the genomes of intracellular bacteria that are typically considered highly stable and prone to genomic degradation.     

Complete genome sequence of "Candidatus Tremblaya princeps" strain PCVAL, an intriguing translational machine below the living-cell status

The sequence of the genome of "Candidatus Tremblaya princeps" strain PCVAL, the primary endosymbiont of the citrus mealybug Planococcus citri, has been determined. "Ca. Tremblaya princeps" presents an unusual nested endosymbiosis and harbors a gammaproteobacterial symbiont within its cytoplasm in all analyzed mealybugs. The genome sequence reveals that "Ca. Tremblaya princeps" cannot be considered an independent organism but that the consortium with its gammaproteobacterial symbiotic associate represents a new composite living being.     

Host hybridization as a potential mechanism of lateral symbiont transfer in deep‐sea vesicomyid clams

Deep‐sea vesicomyid clams live in mutualistic symbiosis with chemosynthetic bacteria that are inherited through the maternal germ line. On evolutionary timescales, strictly vertical transmission should lead to cospeciation of host mitochondrial and symbiont lineages; nonetheless, examples of incongruent phylogenies have been reported, suggesting that symbionts are occasionally horizontally transmitted between host species. The current paradigm for vesicomyid clams holds that direct transfers cause host shifts or mixtures of symbionts. An alternative hypothesis suggests that hybridization between host species might explain symbiont transfers. Two clam species, Archivesica gigas and Phreagena soyoae, frequently co‐occur at deep‐sea hydrocarbon seeps in the eastern Pacific Ocean. Although the two species typically host gammaproteobacterial symbiont lineages marked by divergent 16S rRNA phylotypes, we identified a number of clams with the A. gigas mitotype that hosted symbionts with the P. soyoae phylotype. Demographic inference models based on genome‐wide SNP data and three Sanger sequenced gene markers provided evidence that A. gigas and P. soyoae hybridized in the past, supporting the hypothesis that hybridization might be a viable mechanism of interspecific symbiont transfer. These findings provide new perspectives on the evolution of vertically transmitted symbionts and their hosts in deep‐sea chemosynthetic environments.     

Endosymbioses between bacteria and deep-sea siboglinid tubeworms from an Arctic Cold Seep (Haakon Mosby Mud Volcano, Barents Sea)

Siboglinid tubeworms do not have a mouth or gut and live in obligate associations with bacterial endosymbionts. Little is currently known about the phylogeny of frenulate and moniliferan siboglinids and their symbionts. In this study, we investigated the symbioses of two co-occurring siboglinid species from a methane emitting mud volcano in the Arctic Ocean (Haakon Mosby Mud Volcano, HMMV): Oligobrachia haakonmosbiensis (Frenulata) and Sclerolinum contortum (Monilifera). Comparative sequence analysis of the host-specific 18S and the symbiont-specific 16S rRNA genes of S. contortum showed that the close phylogenetic relationship of this host to vestimentiferan siboglinids was mirrored in the close relationship of its symbionts to the sulfur-oxidizing gammaproteobacterial symbionts of vestimentiferans. A similar congruence between host and symbiont phylogeny was observed in O. haakonmosbiensis: both this host and its symbionts were most closely related to the frenulate siboglinid O. mashikoi and its gammaproteobacterial symbiont. The symbiont sequences from O. haakonmosbiensis and O. mashikoi formed a clade unaffiliated with known methane- or sulfur-oxidizing bacteria. Fluorescence in situ hybridization indicated that the dominant bacterial phylotypes originated from endosymbionts residing inside the host trophosome. In both S. contortum and O. haakonmosbiensis, characteristic genes for autotrophy (cbbLM) and sulfur oxidation (aprA) were present, while genes diagnostic for methanotrophy were not detected. The molecular data suggest that both HMMV tubeworm species harbour chemoautotrophic sulfur-oxidizing symbionts. In S. contortum, average stable carbon isotope values of fatty acids and cholesterol of -43 per thousand were highly negative for a sulfur oxidizing symbiosis, but can be explained by a (13)C-depleted CO(2) source at HMMV. In O. haakonmosbiensis, stable carbon isotope values of fatty acids and cholesterol of -70 per thousand are difficult to reconcile with our current knowledge of isotope signatures for chemoautotrophic processes.     

The genome of an endosymbiotic methanogen is very similar to those of its free‐living relatives

The methanogenic endosymbionts of anaerobic protists represent the only known intracellular archaea, yet, almost nothing is known about genome structure and content in these lineages. Here, an almost complete genome of an intracellular Methanobacterium species was assembled from a metagenome derived from its host ciliate, a Heterometopus species. Phylogenomic analysis showed that the endosymbiont was closely related to free‐living Methanobacterium isolates, and when compared with the genomes of free‐living Methanobacterium, the endosymbiont did not show significant reduction in genome size or GC content. Additionally, the Methanobacterium endosymbiont genome shared the majority of its genes with its closest relative, though it did also contain unique genes possibly involved in interactions with the host via membrane‐associated proteins, the removal of toxic by‐products from host metabolism and the production of small signalling molecules. Though anaerobic ciliates have been shown to transmit their endosymbionts to daughter cells during division, the results presented here could suggest that the endosymbiotic Methanobacterium did not experience significant genetic isolation or drift and/or that this lineage was only recently acquired. Altogether, comparative genomic analysis identified genes potentially involved in the establishment and maintenance of the symbiosis, as well provided insight into the genomic consequences for an intracellular archaeum.     

Complete genome sequence of Candidatus Ruthia magnifica

The hydrothermal vent clam Calyptogena magnifica (Bivalvia: Mollusca) is a member of the Vesicomyidae. Species within this family form symbioses with chemosynthetic Gammaproteobacteria. They exist in environments such as hydrothermal vents and cold seeps and have a rudimentary gut and feeding groove, indicating a large dependence on their endosymbionts for nutrition. The C. magnifica symbiont, Candidatus Ruthia magnifica, was the first intracellular sulfur-oxidizing endosymbiont to have its genome sequenced (Newton et al. 2007). Here we expand upon the original report and provide additional details complying with the emerging MIGS/MIMS standards. The complete genome exposed the genetic blueprint of the metabolic capabilities of the symbiont. Genes which were predicted to encode the proteins required for all the metabolic pathways typical of free-living chemoautotrophs were detected in the symbiont genome. These include major pathways including carbon fixation, sulfur oxidation, nitrogen assimilation, as well as amino acid and cofactor/vitamin biosynthesis. This genome sequence is invaluable in the study of these enigmatic associations and provides insights into the origin and evolution of autotrophic endosymbiosis.     

Swapping symbionts in spittlebugs: evolutionary replacement of a reduced genome symbiont

Bacterial symbionts that undergo long-term maternal transmission experience elevated fixation of deleterious mutations, resulting in massive loss of genes and changes in gene sequences that appear to limit efficiency of gene products. Potentially, this dwindling of symbiont functionality impacts hosts that depend on these bacteria for nutrition. One evolutionary escape route is the acquisition of a novel symbiont with a robust genome and metabolic capabilities. Such an acquisition has occurred in an ancestor of Philaenus spumarius, the meadow spittlebug (Insecta: Cercopoidea), which has replaced its ancient association with the tiny genome symbiont Zinderia insecticola (Betaproteobacteria) with an association with a symbiont related to Sodalis glossinidius (Gammaproteobacteria). Spittlebugs feed exclusively on xylem sap, a diet that is low both in essential amino acids and in sugar or other substrates for energy production. The new symbiont genome has undergone proliferation of mobile elements resulting in many gene inactivations; nonetheless, it has selectively maintained genes replacing functions of its predecessor for amino-acid biosynthesis. Whereas ancient symbiont partners typically retain perfectly complementary sets of amino-acid biosynthetic pathways, the novel symbiont introduces some redundancy as it retains some pathways also present in the partner symbionts (Sulcia muelleri). Strikingly, the newly acquired Sodalis-like symbiont retains genes underlying efficient routes of energy production, including a complete TCA cycle, potentially relaxing the severe energy limitations of the xylem-feeding hosts. Although evolutionary replacements of ancient symbionts are infrequent, they potentially enable evolutionary and ecological novelty by conferring novel metabolic capabilities to host lineages.     

Genomic signatures of obligate host dependence in the luminous bacterial symbiont of a vertebrate

The majority of bacteria engaged in bioluminescent symbiosis are environmentally acquired and facultatively symbiotic. A few enigmatic bioluminescent symbionts have not been successfully cultured, which has led to speculation that they may be obligately dependent on their hosts. Here, we report the draft genome of the uncultured luminous symbiont of an anomalopid flashlight fish, ‘Candidatus Photodesmus katoptron’. The genome of the anomalopid symbiont is reduced by 80% compared with close relatives and lacks almost all genes necessary for amino acid synthesis and for metabolism of energy sources other than glucose, supporting obligate dependence on the host for growth. ‘Candidatus Photodesmus katoptron’ is the first described obligate mutualistic symbiont of a vertebrate. Unlike most other obligate mutualists, the anomalopid symbiont genome has retained complete pathways for chemotaxis and motility as well as most genes involved in cell wall production, consistent with the hypothesis that these bacteria may be transmitted environmentally during an extra‐host phase.     

Population structure, levels of selection, and the evolution of intracellular symbionts

Many obligately intracellular symbionts exhibit a characteristic set of genetic changes that include an increase in substitution rates, loss of many genes, and apparent destabilization of many proteins and structural RNAs. Authors have suggested that these changes are due to increased mutation rates, or, more commonly, decreased effective population size due to population bottlenecks at the symbiont or, perhaps, host level. I propose that the increase in substitution rates and accumulation of deleterious mutations is a consequence of the population structure imposed on the endosymbionts by strict host association, loss of horizontal transmission and potentially conflicting levels of selection. I analyze a population genetic model of endosymbiont evolution, and demonstrate that substitution rates will increase, and the effect of those substitutions on endosymbiont fitness will become more deleterious as horizontal transmission among hosts decreases. Additionally, I find that there is a critical level of horizontal transmission below which natural selection cannot effectively purge deleterious mutations, leading to an expected loss of fitness over time. This critical level varies across loci with the degree of correlation between host and endosymbiont fitness, and may help explain differential retention and loss of certain genes.     

Novel Chemoautotrophic Endosymbiosis between a Member of the Epsilonproteobacteria and the Hydrothermal-Vent Gastropod Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean

The hydrothermal-vent gastropod Alviniconcha aff. hessleri from the Kairei hydrothermal field on the Central Indian Ridge houses bacterium-like cells internally in its greatly enlarged gill. A single 16S rRNA gene sequence was obtained from the DNA extract of the gill, and phylogenetic analysis placed the source organism within a lineage of the epsilon subdivision of the Proteobacteria. Fluorescence in situ hybridization analysis with an oligonucleotide probe targeting the specific epsilonproteobacterial subgroup showed the bacterium densely colonizing the gill filaments. Carbon isotopic homogeneity among the gastropod tissue parts, regardless of the abundance of the endosymbiont cells, suggests that the carbon isotopic composition of the endosymbiont biomass is approximately the same as that of the gastropod. Compound-specific carbon isotopic analysis revealed that fatty acids from the gastropod tissues are all ¹³C enriched relative to the gastropod biomass and that the monounsaturated C₁₆ fatty acid that originates from the endosymbiont is as ¹³C enriched relative to the gastropod biomass as that of the epsilonproteobacterial cultures grown under chemoautotrophic conditions. This fractionation pattern is most likely due to chemoautotrophy based on the reductive tricarboxylic-acid (rTCA) cycle and subsequent fatty acid biosynthesis from ¹³C-enriched acetyl coenzyme A. Enzymatic characterization revealed evident activity of several key enzymes of the rTCA cycle, as well as the absence of ribulose-1,5-bisphosphate carboxylase/oxygenase activity in the gill tissue. The results from anatomic, molecular phylogenetic, bulk and compound-specific carbon isotopic, and enzymatic analyses all support the inference that a novel nutritional strategy relying on chemoautotrophy in the epsilonproteobacterial endosymbiont is utilized by the hydrothermal-vent gastropod from the Indian Ocean. The discrepancies between the data of the present study and those of previous ones for Alviniconcha gastropods from the Pacific Ocean imply that at least two lineages of chemoautotrophic bacteria, phylogenetically distinct at the subdivision level, occur as the primary endosymbiont in one host animal type.     

Comparative Genomics of Wolbachia and the Bacterial Species Concept

The importance of host-specialization to speciation processes in obligate host-associated bacteria is well known, as is also the ability of recombination to generate cohesion in bacterial populations. However, whether divergent strains of highly recombining intracellular bacteria, such as Wolbachia, can maintain their genetic distinctness when infecting the same host is not known. We first developed a protocol for the genome sequencing of uncultivable endosymbionts. Using this method, we have sequenced the complete genomes of the Wolbachia strains wHa and wNo, which occur as natural double infections in Drosophila simulans populations on the Seychelles and in New Caledonia. Taxonomically, wHa belong to supergroup A and wNo to supergroup B. A comparative genomics study including additional strains supported the supergroup classification scheme and revealed 24 and 33 group-specific genes, putatively involved in host-adaptation processes. Recombination frequencies were high for strains of the same supergroup despite different host-preference patterns, leading to genomic cohesion. The inferred recombination fragments for strains of different supergroups were of short sizes, and the genomes of the co-infecting Wolbachia strains wHa and wNo were not more similar to each other and did not share more genes than other A- and B-group strains that infect different hosts. We conclude that Wolbachia strains of supergroup A and B represent genetically distinct clades, and that strains of different supergroups can co-exist in the same arthropod host without converging into the same species. This suggests that the supergroups are irreversibly separated and that barriers other than host-specialization are able to maintain distinct clades in recombining endosymbiont populations. Acquiring a good knowledge of the barriers to genetic exchange in Wolbachia will advance our understanding of how endosymbiont communities are constructed from vertically and horizontally transmitted genes.     

Evolution of symbiotic organs and endosymbionts in lygaeid stinkbugs

We investigated seed bugs of the genus Nysius (Insecta: Hemiptera: Lygaeidae) for their symbiotic bacteria. From all the samples representing 4 species, 18 populations and 281 individuals, specific bacterial 16S rRNA gene sequences were consistently identified, which formed a distinct clade in the Gammaproteobacteria. In situ hybridization showed that the bacterium was endocellularly localized in a pair of large bacteriomes that were amorphous in shape, deep red in color, and in association with gonads. In the ovary of adult females, the endosymbiont was also localized in the ‘infection zone'' in the middle of each germarium and in the ‘symbiont ball'' at the anterior pole of each oocyte, indicating vertical transmission of the endosymbiont through the ovarial passage. Phylogenetic analyses based on bacterial 16S rRNA, groEL and gyrB genes consistently supported a coherent monophyly of the Nysius endosymbionts. The possibility of a sister relationship to ‘Candidatus Kleidoceria schneideri'', the bacteriome-associated endosymbiont of a lygaeid bug Kleidocerys resedae, was statistically rejected, indicating independent evolutionary origins of the endosymbionts in the Lygaeidae. The endosymbiont genes consistently exhibited AT-biased nucleotide compositions and accelerated rates of molecular evolution, and the endosymbiont genome was only 0.6 Mb in size. The endosymbiont phylogeny was congruent with the host insect phylogeny, suggesting strict vertical transmission and host–symbiont co-speciation over evolutionary time. Based on these results, we discuss the evolution of bacteriomes and endosymbionts in the Heteroptera, most members of which are associated with gut symbiotic bacteria. The designation ‘Candidatus Schneideria nysicola'' is proposed for the endosymbiont clade.     

Endosymbiont population genomics sheds light on transmission mode,partner specificity,and stability of the scaly-foot snail holobiont

The scaly-foot snail (Chrysomallon squamiferum) inhabiting deep-sea hydrothermal vents in the Indian Ocean relies on its sulphur-oxidising gammaproteobacterial endosymbionts for nutrition and energy. In this study, we investigate the specificity, transmission mode, and stability of multiple scaly-foot snail populations dwelling in five vent fields with considerably disparate geological, physical and chemical environmental conditions. Results of population genomics analyses reveal an incongruent phylogeny between the endosymbiont and mitochondrial genomes of the scaly-foot snails in the five vent fields sampled, indicating that the hosts obtain endosymbionts via horizontal transmission in each generation. However, the genetic homogeneity of many symbiont populations implies that vertical transmission cannot be ruled out either. Fluorescence in situ hybridisation of ovarian tissue yields symbiont signals around the oocytes, suggesting that vertical transmission co-occurs with horizontal transmission. Results of in situ environmental measurements and gene expression analyses from in situ fixed samples show that the snail host buffers the differences in environmental conditions to provide the endosymbionts with a stable intracellular micro-environment, where the symbionts serve key metabolic functions and benefit from the host’s cushion. The mixed transmission mode, symbiont specificity at the species level, and stable intracellular environment provided by the host support the evolutionary, ecological, and physiological success of scaly-foot snail holobionts in different vents with unique environmental parameters.Subject terms: Bacterial genomics, Marine microbiology, Symbiosis     

Chemosynthetic endosymbioses: adaptations to oxic-anoxic interfaces

Chemosynthetic endosymbioses occur ubiquitously at oxic-anoxic interfaces in marine environments. In these mutualisms, bacteria living directly within the cell of a eukaryotic host oxidize reduced chemicals (sulfur or methane), fueling their own energetic and biosynthetic needs, in addition to those of their host. In habitats such as deep-sea hydrothermal vents, chemosynthetic symbioses dominate the biomass, contributing substantially to primary production. Although these symbionts have yet to be cultured, physiological, biochemical and molecular approaches have provided insights into symbiont genetics and metabolism, as well as into symbiont-host interactions, adaptations and ecology. Recent studies of endosymbiont biology are reviewed, with emphasis on a conceptual model of thioautotrophic metabolism and studies linking symbiont physiology with the geochemical environment. We also discuss current and future research directions, focusing on the use of genome analyses to reveal mechanisms that initiate and sustain the symbiont-host interaction.     

Pyrosequencing analysis of endosymbiont population structure: co-occurrence of divergent symbiont lineages in a single vesicomyid host clam

Bacteria–eukaryote endosymbioses are perhaps the most pervasive co-evolutionary associations in nature. Here, intracellular chemosynthetic symbionts of deep-sea clams ( Vesicomyidae ) were analysed by amplicon pyrosequencing to explore how symbiont transmission mode affects the genetic diversity of the within-host symbiont population. Vesicomyid symbionts ( Gammaproteobacteria ) are presumed to be obligately intracellular, to undergo nearly strict vertical transmission between host generations, and to be clonal within a host. However, recent data show that vesicomyid symbionts can be acquired laterally via horizontal transfer between hosts or uptake from the environment, potentially creating opportunities for multiple symbiont strains to occupy the same host. Here, genotype-specific PCR and direct sequencing of the bacterial internal transcribed spacer initially demonstrated the co-occurrence of two symbiont strains, symA and symB (93.5% nt identity), in 8 of 118 Vesicomya sp. clams from 3 of 7 hydrothermal vent sites on the Juan de Fuca Ridge. To confirm multiple strains within individual clams, amplicon pyrosequencing of two symbiont loci was used to obtain deep-coverage measurements (mean: ∼1500× coverage per locus per clam) of symbiont population structure. Pyrosequencing confirmed symA–symB co-occurrence for two individuals, showing the presence of both genotypes in amplicon pools. However, in the majority of clams, the endosymbiont population was remarkably homogenous, with > 99.5% of sequences collapsing into a single symbiont genotype in each clam. These results support the hypothesis that a predominantly vertical transmission strategy leads to the fixation of a single symbiont strain in most hosts. However, mixed symbiont populations do occur in vesicomyids, potentially facilitating the exchange of genetic material between divergent symbiont lineages.     

Loss of DNA recombinational repair enzymes in the initial stages of genome degeneration

Many obligate intracellular pathogens and symbionts undergo genome degeneration during long-term association with eukaryotic hosts; however, very little is known about genome changes that occur in the initial stages of such intracellular associations. By focusing on a clade of bacteria that have recently established symbiotic associations with insect hosts, we have identified events that may contribute to the reduction and degeneration of symbiont genomes. Unlike virtually all other bacteria, the obligate symbionts of maize and rice weevils each display substantial sequence divergence between multiple copies of their rDNA genes, resulting from a reduction in the efficacy of recombinational gene conversion, coincident with the inactivation of the recombinational repair gene recF in the common ancestor of both symbionts. The maize weevil endosymbiont also lacks a functional recA, resulting in further reduction in the efficacy of gene conversion between paralogous rDNAs and in a novel IS-mediated deletion in a 23S rDNA gene. Similar events may be pervasive during the evolution of symbiosis because symbiont genomes typically lack recombinational repair genes and have reduced numbers of ribosomal operons.     

Genome Sequence Analysis Indicates that the Model Eukaryote Nematostella vectensis Harbors Bacterial Consorts

Analysis of the genome sequence of the starlet sea anemone, Nematostella vectensis, reveals many genes whose products are phylogenetically closer to proteins encoded by bacteria or bacteriophages than to any metazoan homologs. One explanation for such sequence affinities could be that these genes have been horizontally transferred from bacteria to the Nematostella lineage. We show, however, that bacterium-like and phage-like genes sequenced by the N. vectensis genome project tend to cluster on separate scaffolds, which typically do not include eukaryotic genes and differ from the latter in their GC contents. Moreover, most of the bacterium-like genes in N. vectensis either lack introns or the introns annotated in such genes are false predictions that, when translated, often restore the missing portions of their predicted protein products. In a freshwater cnidarian, Hydra, for which a proteobacterial endosymbiont is known, these gene features have been used to delineate the DNA of that endosymbiont sampled by the genome sequencing project. We predict that a large fraction of bacterium-like genes identified in the N. vectensis genome similarly are drawn from the contemporary bacterial consorts of the starlet sea anemone. These uncharacterized bacteria associated with N. vectensis are a proteobacterium and a representative of the phylum Bacteroidetes, each represented in the database by an apparently random sample of informational and operational genes. A substantial portion of a putative bacteriophage genome was also detected, which would be especially unlikely to have been transferred to a eukaryote.     

High‐contiguity genome assembly of the chemosynthetic gammaproteobacterial endosymbiont of the cold seep tubeworm Lamellibrachia barhami

Symbiotic relationships between vestimentiferan tubeworms and chemosynthetic Gammaproteobacteria build the foundations of many hydrothermal vent and hydrocarbon seep ecosystems in the deep sea. The association between the vent tubeworm Riftia pachyptila and its endosymbiont Candidatus Endoriftia persephone has become a model system for symbiosis research in deep‐sea vestimentiferans, while markedly fewer studies have investigated symbiotic relationships in other tubeworm species, especially at cold seeps. Here we sequenced the endosymbiont genome of the tubeworm Lamellibrachia barhami from a cold seep in the Gulf of California, using short‐ and long‐read sequencing technologies in combination with Hi‐C and Dovetail Chicago libraries. Our final assembly had a size of ~4.17 MB, a GC content of 54.54%, 137X coverage, 4153 coding sequences, and a CheckM completeness score of 97.19%. A single scaffold contained 99.51% of the genome. Comparative genomic analyses indicated that the L. barhami symbiont shares a set of core genes and many metabolic pathways with other vestimentiferan symbionts, while containing 433 unique gene clusters that comprised a variety of transposases, defence‐related genes and a lineage‐specific CRISPR/Cas3 system. This assembly represents the most contiguous tubeworm symbiont genome resource to date and will be particularly valuable for future comparative genomic studies investigating structural genome evolution, physiological adaptations and host‐symbiont communication in chemosynthetic animal‐microbe symbioses.     

Symbiotic origin of a novel actin gene in the cryptophyte Pyrenomonas helgolandii

Cryptophytes are photosynthetic protists that have acquired their plastids through the secondary symbiotic uptake of a red alga. A remarkable feature of cryptophytes is that they maintain a reduced form of the red algal nucleus, the nucleomorph, between the second and third plastid membranes (periplastidial compartment; PC). The nucleomorph is thought to be a transition state in the evolution of secondary plastids, with this genome ultimately being lost when photosynthesis comes under full control of the "host" nucleus (e.g., as in heterokonts, haptophytes, and euglenophytes). Genes presently found in the nucleomorph seem to be restricted to those involved in its own maintenance and to that of the plastid; other genes were lost as the endosymbiont was progressively reduced to its present state. Surprisingly, we found that the cryptophyte Pyrenomonas helgolandii possesses a novel type of actin gene that originated from the nucleomorph genome of the symbiont. Our results demonstrate for the first time that secondary symbionts can contribute genes to the host lineage which are unrelated to plastid function. These genes are akin to the products of gene duplication or lateral transfer and provide a source of evolutionary novelty that can significantly increase the genetic diversity of the host lineage. We postulate that this may be a common phenomenon in algae containing secondary plastids that has yet to be fully appreciated due to a dearth of evolutionary studies of nuclear genes in these taxa.