A widespread coral-infecting apicomplexan with chlorophyll biosynthesis genes.

Apicomplexa is a group of obligate intracellular parasites that includes the causative agents of human diseases such as malaria and toxoplasmosis. Apicomplexans evolved from free-living phototrophic ancestors, but how this transition to parasitism occurred remains unknown. One potential clue lies in coral reefs, of which environmental DNA surveys have uncovered several lineages of uncharacterized basally branching apicomplexans1,2. Reef-building corals have a well-studied symbiotic relationship with photosynthetic Symbiodiniaceae dinoflagellates (for example, Symbiodinium3), but the identification of other key microbial symbionts of corals has proven to be challenging4,5. Here we use community surveys, genomics and microscopy analyses to identify an apicomplexan lineage-which we informally name 'corallicolids'-that was found at a high prevalence (over 80% of samples, 70% of genera) across all major groups of corals. Corallicolids were the second most abundant coral-associated microeukaryotes after the Symbiodiniaceae, and are therefore core members of the coral microbiome. In situ fluorescence and electron microscopy confirmed that corallicolids live intracellularly within the tissues of the coral gastric cavity, and that they possess apicomplexan ultrastructural features. We sequenced the genome of the corallicolid plastid, which lacked all genes for photosystem proteins; this indicates that corallicolids probably contain a non-photosynthetic plastid (an apicoplast6). However, the corallicolid plastid differs from all other known apicoplasts because it retains the four ancestral genes that are involved in chlorophyll biosynthesis. Corallicolids thus share characteristics with both their parasitic and their free-living relatives, which suggests that they are evolutionary intermediates and implies the existence of a unique biochemistry during the transition from phototrophy to parasitism.

Reconstruction of Plastid Proteomes of Apicomplexans and Close Relatives Reveals the Major Evolutionary Outcomes of Cryptic Plastids.

Apicomplexans and related lineages comprise many obligate symbionts of animals; some of which cause notorious diseases such as malaria. They evolved from photosynthetic ancestors and transitioned into a symbiotic lifestyle several times, giving rise to species with diverse non-photosynthetic plastids. Here, we sought to reconstruct the evolution of the cryptic plastids in the apicomplexans, chrompodellids, and squirmids (ACS clade) by generating five new single-cell transcriptomes from understudied gregarine lineages, constructing a robust phylogenomic tree incorporating all ACS clade sequencing datasets available, and using these to examine in detail, the evolutionary distribution of all 162 proteins recently shown to be in the apicoplast by spatial proteomics in Toxoplasma. This expanded homology-based reconstruction of plastid proteins found in the ACS clade confirms earlier work showing convergence in the overall metabolic pathways retained once photosynthesis is lost, but also reveals differences in the degrees of plastid reduction in specific lineages. We show that the loss of the plastid genome is common and unexpectedly find many lineage- and species-specific plastid proteins, suggesting the presence of evolutionary innovations and neofunctionalizations that may confer new functional and metabolic capabilities that are yet to be discovered in these enigmatic organelles.

Phylogenomics reveals Adeleorina are an ancient and distinct subgroup of Apicomplexa.

Apicomplexans are a diverse phylum of unicellular eukaryotes that share obligate relationships with terrestrial and aquatic animal hosts. Many well-studied apicomplexans are responsible for several deadly zoonotic and human diseases, most notably malaria caused by Plasmodium. Interest in the evolutionary origin of apicomplexans has also spurred recent work on other more deeply-branching lineages, especially gregarines and sister groups like squirmids and chrompodellids. But a full picture of apicomplexan evolution is still lacking several lineages, and one major, diverse lineage that is notably absent is the adeleorinids. Adeleorina apicomplexans comprises hundreds of described species that infect invertebrate and vertebrate hosts across the globe. Although historically considered coccidians, phylogenetic trees based on limited data have shown conflicting branch positions for this subgroup, leaving this question unresolved. Phylogenomic trees and large-scale analyses comparing cellular functions and metabolism between major subgroups of apicomplexans have not incorporated Adeleorina because only a handful of molecular markers and a couple organellar genomes are available, ultimately excluding this group from contributing to our understanding of apicomplexan evolution and biology. To address this gap, we have generated complete genomes from mitochondria and plastids, as well as multiple deep-coverage single-cell transcriptomes of nuclear genes from two Adeleorina species, Klossia helicina and Legerella nova, and inferred a 206-protein phylogenomic tree of Apicomplexa. We observed distinct structures reported in species descriptions as remnant host structures surrounding adeleorinid oocysts. Klossia helicina and L. nova branched, as expected, with monoxenous adeleorinids within the Adeleorina and their mitochondrial and plastid genomes exhibited similarity to published organellar adeleorinid genomes. We show with a phylogeneomic tree and subsequent phylogenomic analyses that Adeleorina are not closely related to any of the currently sampled apicomplexan subgroups, and instead fall as a sister to a large clade encompassing Coccidia, Protococcidia, Hematozoa, and Nephromycida, collectively. This resolves Adeleorina as a key independently-branching group, separate from coccidians, on the tree of Apicomplexa, which now has all known major lineages sampled.

Division of labor in honey bee gut microbiota for plant polysaccharide digestion.

Bees acquire carbohydrates from nectar and lipids; and amino acids from pollen, which also contains polysaccharides including cellulose, hemicellulose, and pectin. These potential energy sources could be degraded and fermented through microbial enzymatic activity, resulting in short chain fatty acids available to hosts. However, the contributions of individual microbiota members to polysaccharide digestion have remained unclear. Through analysis of bacterial isolate genomes and a metagenome of the honey bee gut microbiota, we identify that Bifidobacterium and Gilliamella are the principal degraders of hemicellulose and pectin. Both Bifidobacterium and Gilliamella show extensive strain-level diversity in gene repertoires linked to polysaccharide digestion. Strains from honey bees possess more such genes than strains from bumble bees. In Bifidobacterium, genes encoding carbohydrate-active enzymes are colocated within loci devoted to polysaccharide utilization, as in Bacteroides from the human gut. Carbohydrate-active enzyme-encoding gene expressions are up-regulated in response to particular hemicelluloses both in vitro and in vivo. Metabolomic analyses document that bees experimentally colonized by different strains generate distinctive gut metabolomic profiles, with enrichment for specific monosaccharides, corresponding to predictions from genomic data. The other 3 core gut species clusters (Snodgrassella and 2 Lactobacillus clusters) possess few or no genes for polysaccharide digestion. Together, these findings indicate that strain composition within individual hosts determines the metabolic capabilities and potentially affects host nutrition. Furthermore, the niche specialization revealed by our study may promote overall community stability in the gut microbiomes of bees.

Taxonomy of the Apicomplexan Symbionts of Coral, including Corallicolida ord. nov., Reassignment of the Genus Gemmocystis, and Description of New Species Corallicola aquarius gen. nov. sp. nov. and Anthozoaphila gnarlus gen. nov. sp. nov.

Corals (Metazoa; Cnidaria; Anthozoa) have recently been shown to play host to a widespread and diverse group of intracellular symbionts of the phylum Apicomplexa. These symbionts, colloquially called "corallicolids", are mostly known through molecular analyses, and no formal taxonomy has been proposed. Another apicomplexan, Gemmocystis cylindrus (described from the coral Dendrogyra cylindrus), may be related to corallicolids, but lacks molecular data. Here, we isolate and describe motile trophozoite (feeding) corallicolids cells using microscopic (light, SEM, and TEM) and molecular phylogenetic analysis to provide the basis for a formal description. Phylogenetic analyses using nuclear and plastid rRNA operons, and three mitochondrial protein sequences derived from single cell transcriptomes, all confirm that these organisms fall into a discrete deep-branching clade within the Apicomplexa not closely related to any known species or major subgroup. As a result, we assign this clade to a new order, Corallicolida ord. nov., and family, Corallicolidae fam. nov. We describe a type species, Corallicola aquarius gen. nov. sp. nov. from its Rhodactis sp. host, and also describe a second species, Anthozoaphila gnarlus gen. nov. sp. nov., from the coral host Madracis mirabilis. Finally, we propose reassigning the incertae sedis taxon G. cylindrus from the order Agamococcidiorida to the Corallicolida, based on similarities in morphology and host localization to that of the corallicolids.

Genome-wide screen identifies host colonization determinants in a bacterial gut symbiont.

Animal guts are often colonized by host-specialized bacterial species to the exclusion of other transient microorganisms, but the genetic basis of colonization ability is largely unknown. The bacterium Snodgrassella alvi is a dominant gut symbiont in honey bees, specialized in colonizing the hindgut epithelium. We developed methods for transposon-based mutagenesis in S. alvi and, using high-throughput DNA sequencing, screened genome-wide transposon insertion (Tn-seq) and transcriptome (RNA-seq) libraries to characterize both the essential genome and the genes facilitating host colonization. Comparison of Tn-seq results from laboratory cultures and from monoinoculated worker bees reveal that 519 of 2,226 protein-coding genes in S. alvi are essential in culture, whereas 399 are not essential but are beneficial for gut colonization. Genes facilitating colonization fall into three broad functional categories: extracellular interactions, metabolism, and stress responses. Extracellular components with strong fitness benefits in vivo include trimeric autotransporter adhesins, O antigens, and type IV pili (T4P). Experiments with T4P mutants establish that T4P in S. alvi likely function in attachment and biofilm formation, with knockouts experiencing a competitive disadvantage in vivo. Metabolic processes promoting colonization include essential amino acid biosynthesis and iron acquisition pathways, implying nutrient scarcity within the hindgut environment. Mechanisms to deal with various stressors, such as for the repair of double-stranded DNA breaks and protein quality control, are also critical in vivo. This genome-wide study identifies numerous genetic networks underlying colonization by a gut commensal in its native host environment, including some known from more targeted studies in other host-microbe symbioses.

Microbiome Structure Influences Infection by the Parasite Crithidia bombi in Bumble Bees.

Recent declines in bumble bee populations are of great concern and have prompted critical evaluations of the role of pathogen introductions and host resistance in bee health. One factor that may influence host resilience when facing infection is the gut microbiota. Previous experiments with Bombus terrestris, a European bumble bee, showed that the gut microbiota can protect against Crithidia bombi, a widespread trypanosomatid parasite of bumble bees. However, the particular characteristics of the microbiome responsible for this protective effect have thus far eluded identification. Using wild and commercially sourced Bombus impatiens, an important North American pollinator, we conducted cross-wise microbiota transplants to naive hosts of both backgrounds and challenged them with a Crithidia parasite. As with B. terrestris, we find that microbiota-dependent protection against Crithidia operates in B. impatiens Lower Crithidia infection loads were experimentally associated with high microbiome diversity, large gut bacterial populations, and the presence of Apibacter, Lactobacillus Firm-5, and Gilliamella spp. in the gut community. These results indicate that even subtle differences between gut community structures can have a significant impact on a microbiome's ability to defend against parasite infections.IMPORTANCE Many wild bumble bee populations are under threat due to human activity, including through the introduction of pathogens via commercially raised bees. Recently, it was found that the bumble bee gut microbiota can help defend against a common parasite, Crithidia bombi, but the particular factors contributing to this protection are unknown. Using both wild and commercially raised bees, we conducted microbiota transplants to show that microbiome diversity, total gut bacterial load, and the presence of certain core members of the microbiota may all impact bee susceptibility to Crithidia infection. Bee origin (genetic background) was also a factor. Finally, by examining this phenomenon in a previously uninvestigated bee species, our study demonstrates that microbiome-mediated resistance to Crithidia is conserved across multiple bumble bee species. These findings highlight how intricate interactions between hosts, microbiomes, and parasites can have wide-ranging consequences for the health of ecologically important species.

Genomics and host specialization of honey bee and bumble bee gut symbionts.

Gilliamella apicola and Snodgrassella alvi are dominant members of the honey bee (Apis spp.) and bumble bee (Bombus spp.) gut microbiota. We generated complete genomes of the type strains G. apicola wkB1(T) and S. alvi wkB2(T) (isolated from Apis), as well as draft genomes for four other strains from Bombus. G. apicola and S. alvi were found to occupy very different metabolic niches: The former is a saccharolytic fermenter, whereas the latter is an oxidizer of carboxylic acids. Together, they may form a syntrophic network for partitioning of metabolic resources. Both species possessed numerous genes [type 6 secretion systems, repeats in toxin (RTX) toxins, RHS proteins, adhesins, and type IV pili] that likely mediate cell-cell interactions and gut colonization. Variation in these genes could account for the host fidelity of strains observed in previous phylogenetic studies. Here, we also show the first experimental evidence, to our knowledge, for this specificity in vivo: Strains of S. alvi were able to colonize their native bee host but not bees of another genus. Consistent with specific, long-term host association, comparative genomic analysis revealed a deep divergence and little or no gene flow between Apis and Bombus gut symbionts. However, within a host type (Apis or Bombus), we detected signs of horizontal gene transfer between G. apicola and S. alvi, demonstrating the importance of the broader gut community in shaping the evolution of any one member. Our results show that host specificity is likely driven by multiple factors, including direct host-microbe interactions, microbe-microbe interactions, and social transmission.

Apibacter adventoris gen. nov., sp. nov., a member of the phylum Bacteroidetes isolated from honey bees.

Honey bees and bumble bees harbour a small, defined set of gut bacterial associates. Strains matching sequences from 16S rRNA gene surveys of bee gut microbiotas were isolated from two honey bee species from East Asia. These isolates were mesophlic, non-pigmented, catalase-positive and oxidase-negative. The major fatty acids were iso-C15 : 0, iso-C17 : 0 3-OH, C16 : 0 and C16 : 0 3-OH. The DNA G+C content was 29-31 mol%. They had ∼87 % 16S rRNA gene sequence identity to the closest relatives described. Phylogenetic reconstruction using 20 protein-coding genes showed that these bee-derived strains formed a highly supported monophyletic clade, sister to the clade containing species of the genera Chryseobacterium and Elizabethkingia within the family Flavobacteriaceae of the phylum Bacteroidetes. On the basis of phenotypic and genotypic characteristics, we propose placing these strains in a novel genus and species: Apibacter adventoris gen. nov., sp. nov. The type strain of Apibacter adventoris is wkB301T ( = NRRL B-65307T = NCIMB 14986T).

Complete genome sequences of 12 bacterial strains from the honey bee gut, resolved with long-read nanopore sequencing.

We report the de novo sequencing of six bacterial strains isolated from the Western honey bee, as well as the resequencing of six strains that have existing draft genomes, to obtain complete, chromosomal-level assemblies. These strains include the bee gut symbiont genera Bartonella, Bifidobacterium, Snodgrassella, Gilliamella, Lactobacillus, and the opportunistic pathogen Serratia marcescens KZ11.

Coral-infecting parasites in cold marine ecosystems.

Coral reefs are a biodiversity hotspot,1,2 and the association between coral and intracellular dinoflagellates is a model for endosymbiosis.3,4 Recently, corals and related anthozoans have also been found to harbor another kind of endosymbiont, apicomplexans called corallicolids.5 Apicomplexans are a diverse lineage of obligate intracellular parasites6 that include human pathogens such as the malaria parasite, Plasmodium.7 Global environmental sequencing shows corallicolids are tightly associated with tropical and subtropical reef environments,5,8,9 where they infect diverse corals across a range of depths in many reef systems, and correlate with host mortality during bleaching events.10 All of this points to corallicolids being ecologically significant to coral reefs, but it is also possible they are even more widely distributed because most environmental sampling is biased against parasites that maintain a tight association with their hosts throughout their life cycle. We tested the global distribution of corallicolids using a more direct approach, by specifically targeting potential anthozoan host animals from cold/temperate marine waters outside the coral reef context. We found that corallicolids are in fact common in such hosts, in some cases at high frequency, and that they infect the same tissue as parasites from topical coral reefs. Parasite phylogeny suggests corallicolids move between hosts and habitats relatively frequently, but that biogeography is more conserved. Overall, these results greatly expand the range of corallicolids beyond coral reefs, suggesting they are globally distributed parasites of marine anthozoans, which also illustrates significant blind spots that result from strategies commonly used to sample microbial biodiversity.

Cultivation and characterization of the gut symbionts of honey bees and bumble bees: description of Snodgrassella alvi gen. nov., sp. nov., a member of the family Neisseriaceae of the Betaproteobacteria, and Gilliamella apicola gen. nov., sp. nov., a member of Orbaceae fam. nov., Orbales ord. nov., a sister taxon to the order 'Enterobacteriales' of the Gammaproteobacteria.

Gut-associated bacteria were isolated in axenic culture from the honey bee Apis mellifera and the bumble bees Bombus bimaculatus and B. vagans and are here placed in the novel genera and species Snodgrassella alvi gen. nov., sp. nov. and Gilliamella apicola gen. nov., sp. nov. Two strains from A. mellifera were characterized and are proposed as the type strains of Snodgrassella alvi (type strain wkB2(T) =NCIMB 14803(T) =ATCC BAA-2449(T) =NRRL B-59751(T)) and Gilliamella apicola (type strain wkB1(T) =NCIMB 14804(T) =ATCC BAA-2448(T)), representing, respectively, phylotypes referred to as 'Betaproteobacteria' and 'Gammaproteobacteria-1'/'Gamma-1' in earlier publications. These strains grew optimally under microaerophilic conditions, and did not grow readily under a normal atmosphere. The predominant fatty acids in both strains were palmitic acid (C16:0) and cis-vaccenic acid (C18:1ω7c and/or C18:1ω6c), and both strains had ubiquinone-8 as their major respiratory quinone. The DNA G+C contents were 41.3 and 33.6 mol% for wkB2(T) and wkB1(T), respectively. The Snodgrassella alvi strains from honey bees and bumble bees formed a novel clade within the family Neisseriaceae of the Betaproteobacteria, showing about 94% 16S rRNA gene sequence identity to their closest relatives, species of Stenoxybacter, Alysiella and Kingella. The Gilliamella apicola strains showed the highest 16S rRNA gene sequence identity to Orbus hercynius CN3(T) (93.9%) and several sequences from uncultured insect-associated bacteria. Phylogenetic reconstruction using conserved, single-copy amino acid sequences showed Gilliamella apicola as sister to the order 'Enterobacteriales' of the Gammaproteobacteria. Given its large sequence divergence from and basal position to the well-established order 'Enterobacteriales', we propose to place the clade encompassing Gilliamella apicola and O. hercynius in a new family and order, Orbaceae fam. nov. and Orbales ord. nov.

Frischella perrara gen. nov., sp. nov., a gammaproteobacterium isolated from the gut of the honeybee, Apis mellifera.

The gut of the Western honeybee, Apis mellifera, is colonized by a characteristic set of bacteria. Two distinct gammaproteobacteria are consistent members of this unique microbial community, and one has recently been described in a new genus and species with the name Gilliamella apicola. Here, we present the isolation and characterization of PEB0191(T), a strain belonging to the second gammaproteobacterial species present in the honeybee gut microbiota, formerly referred to as 'Gammaproteobacterium-2'. Cells of strain PEB0191(T) were mesophilic and had a mean length of around 2 µm, and optimal growth was achieved under anaerobic conditions. Growth was not obtained under aerobic conditions and was reduced in a microaerophilic environment. Based on 16S rRNA gene sequence analysis, strain PEB0191(T) belongs to the family Orbaceae, and its closest relatives, with around 95 % sequence similarity, are species of the genera Orbus and Gilliamella. Phylogenetic analyses suggest that PEB0191(T) is more closely related to the genus Orbus than to the genus Gilliamella. In accordance with its evolutionary relationship, further similarities between strain PEB0191(T) and other members of the family Orbaceae were revealed based on the respiratory quinone type (ubiquinone 8), the fatty acid profile and the DNA G+C content. Interestingly, like strains of the genus Gilliamella, PEB0191(T) exhibited a high level of resistance to oxytetracycline. The similar levels of sequence divergence from the genera Gilliamella and Orbus and its uncertain phylogenetic position within the family Orbaceae indicate that strain PEB0191(T) represents a novel species of a new genus, with the proposed name Frischella perrara gen. nov., sp. nov. The type strain of Frischella perrara is PEB0191(T) ( = NCIMB 14821(T) = ATCC BAA-2450(T)).

Gene Transfer Agents in Bacterial Endosymbionts of Microbial Eukaryotes.

Gene transfer agents (GTAs) are virus-like structures that package and transfer prokaryotic DNA from donor to recipient prokaryotic cells. Here, we describe widespread GTA gene clusters in the highly reduced genomes of bacterial endosymbionts from microbial eukaryotes (protists). Homologs of the GTA capsid and portal complexes were initially found to be present in several highly reduced alphaproteobacterial endosymbionts of diplonemid protists (Rickettsiales and Rhodospirillales). Evidence of GTA expression was found in polyA-enriched metatranscriptomes of the diplonemid hosts and their endosymbionts, but due to biases in the polyA-enrichment methods, levels of GTA expression could not be determined. Examining the genomes of closely related bacteria revealed that the pattern of retained GTA head/capsid complexes with missing tail components was common across Rickettsiales and Holosporaceae (Rhodospirillales), all obligate symbionts with a wide variety of eukaryotic hosts. A dN/dS analysis of Rickettsiales and Holosporaceae symbionts revealed that purifying selection is likely the main driver of GTA evolution in symbionts, suggesting they remain functional, but the ecological function of GTAs in bacterial symbionts is unknown. In particular, it is unclear how increasing horizontal gene transfer in small, largely clonal endosymbiont populations can explain GTA retention, and, therefore, the structures may have been repurposed in endosymbionts for host interactions. Either way, their widespread retention and conservation in endosymbionts of diverse eukaryotes suggests an important role in symbiosis.

Host-microbiome metabolism of a plant toxin in bees.

While foraging for nectar and pollen, bees are exposed to a myriad of xenobiotics, including plant metabolites, which may exert a wide range of effects on their health. Although the bee genome encodes enzymes that help in the metabolism of xenobiotics, it has lower detoxification gene diversity than the genomes of other insects. Therefore, bees may rely on other components that shape their physiology, such as the microbiota, to degrade potentially toxic molecules. In this study, we show that amygdalin, a cyanogenic glycoside found in honey bee-pollinated almond trees, can be metabolized by both bees and members of the gut microbiota. In microbiota-deprived bees, amygdalin is degraded into prunasin, leading to prunasin accumulation in the midgut and hindgut. In microbiota-colonized bees, on the other hand, amygdalin is degraded even further, and prunasin does not accumulate in the gut, suggesting that the microbiota contribute to the full degradation of amygdalin into hydrogen cyanide. In vitro experiments demonstrated that amygdalin degradation by bee gut bacteria is strain-specific and not characteristic of a particular genus or species. We found strains of Bifidobacterium, Bombilactobacillus, and Gilliamella that can degrade amygdalin. The degradation mechanism appears to vary since only some strains produce prunasin as an intermediate. Finally, we investigated the basis of degradation in Bifidobacterium wkB204, a strain that fully degrades amygdalin. We found overexpression and secretion of several carbohydrate-degrading enzymes, including one in glycoside hydrolase family 3 (GH3). We expressed this GH3 in Escherichia coli and detected prunasin as a byproduct when cell lysates were cultured with amygdalin, supporting its contribution to amygdalin degradation. These findings demonstrate that both host and microbiota can act together to metabolize dietary plant metabolites.

Most plants produce chemicals that are toxic to at least some animals. Whether or not the toxins are harmful to a particular animal depends on how much they consume and the specific biochemistry that occurs during digestion. The enzymes produced in the gut both by the animal and by the microbes that reside there often help break down toxic substances into less harmful molecules. However, some products of this breakdown can be toxic themselves. While these products can harm the animal, they may also be detrimental to parasites living in the gut, resulting in an overall positive effect. Almonds and their pollen are consumed by humans and bees without apparent harmful effects. However, almonds contain amygdalin, a molecule that can produce the highly toxic compound hydrogen cyanide upon digestion. Although amygdalin can be toxic to bees in high doses, the amount usually found in almond nectar is not harmful, and indeed, it may protect bees from parasites. Motta et al. wanted to know how amygdalin is digested in the gut of bees, and whether gut microbes have a role in this digestion. To answer these questions, Motta et al. compared the effects of consuming amygdalin on normal bees and bees lacking gut microbes. Bees without gut microbes broke down amygdalin into a harmless substance called prunasin. However, only bees with gut microbes could further break down prunasin into hydrogen cyanide. Interestingly, the full metabolism of amygdalin had no detectable effect on whether the bees survived for longer times or on which microbes were found in the gut. Motta et al. also found some gut bacteria in bees that can break down amygdalin and release hydrogen cyanide, and identified the enzyme responsible for the process. When the gene encoding this enzyme was inserted into a different species of bacteria, the second species gained the ability to break down amygdalin. The findings of Motta et al. explain a role of gut microbes in processing amygdalin in bees. In the future, this may be the key to understanding how humans and other creatures process plant toxins. Future work on the relationship between animals and microbes living in their guts could help scientists understand how to manipulate the digestion and processing of toxins, nutrients, or drugs to benefit human health.

Phylogenomics Identifies a New Major Subgroup of Apicomplexans, Marosporida class nov., with Extreme Apicoplast Genome Reduction.

The phylum Apicomplexa consists largely of obligate animal parasites that include the causative agents of human diseases such as malaria. Apicomplexans have also emerged as models to study the evolution of nonphotosynthetic plastids, as they contain a relict chloroplast known as the apicoplast. The apicoplast offers important clues into how apicomplexan parasites evolved from free-living ancestors and can provide insights into reductive organelle evolution. Here, we sequenced the transcriptomes and apicoplast genomes of three deep-branching apicomplexans, Margolisiella islandica, Aggregata octopiana, and Merocystis kathae. Phylogenomic analyses show that these taxa, together with Rhytidocystis, form a new lineage of apicomplexans that is sister to the Coccidia and Hematozoa (the lineages including most medically significant taxa). Members of this clade retain plastid genomes and the canonical apicomplexan plastid metabolism. However, the apicoplast genomes of Margolisiella and Rhytidocystis are the most reduced of any apicoplast, are extremely GC-poor, and have even lost genes for the canonical plastidial RNA polymerase. This new lineage of apicomplexans, for which we propose the class Marosporida class nov., occupies a key intermediate position in the apicomplexan phylogeny, and adds a new complexity to the models of stepwise reductive evolution of genome structure and organelle function in these parasites.

Microbiome Evolution: Having the Guts to Be Different.

Metagenomic sequencing of the gut microbial communities of two closely related bee species, the Western honey bee (Apis mellifera) and the Eastern honey bee (Apis cerana), show that organisms with similar characteristics can harbor unexpected differences in their microbiomes.

Highly Reduced Genomes of Protist Endosymbionts Show Evolutionary Convergence.

Genome evolution in bacterial endosymbionts is notoriously extreme: the combined effects of strong genetic drift and unique selective pressures result in highly reduced genomes with distinctive adaptations to hosts [1-4]. These processes are mostly known from animal endosymbionts, where nutritional endosymbioses represent the best-studied systems. However, eukaryotic microbes, or protists, also harbor diverse bacterial endosymbionts, but their genome reduction and functional relationships with their hosts are largely unexplored [5-7]. We sequenced the genomes of four bacterial endosymbionts from three species of diplonemids, poorly studied but abundant and diverse heterotrophic protists [8-12]. The endosymbionts come from two bacterial families, Rickettsiaceae and Holosporaceae, that have invaded two families of diplonemids, and their genomes have converged on an extremely small size (605-632 kilobase pairs [kbp]), similar gene content (e.g., metabolite transporters and secretion systems), and reduced metabolic potential (e.g., loss of energy metabolism). These characteristics are generally found in both families, but the diplonemid endosymbionts have evolved greater extremes in parallel. They possess modified type VI secretion systems that could function in manipulating host metabolism or other intracellular interactions. Finally, modified cellular machinery like the ATP synthase without oxidative phosphorylation, and the reduced flagellar apparatus present in some diplonemid endosymbionts and nutritional animal endosymbionts, indicates that intracellular mechanisms have converged in bacterial endosymbionts with various functions and from different eukaryotic hosts across the tree of life.