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-Estimated evolutionary history of gene losses in Blattabacterium strains. Blue arrows represent gene loss events related to amino acid biosynthesis. Deficient amino acids or genes caused by each gene loss event are shown with arrow. Time scale is based on a previous estimate by Che et al. (2016).
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Almost all examined cockroaches harbor an obligate intracellular endosymbiont, Blattabacterium cuenoti. On the basis of genome content, Blattabacterium has been inferred to recycle nitrogen wastes and provide amino acids and cofactors for its hosts. Most Blattabacterium strains sequenced to date harbor a genome of ∼630kbp, with the exception of the...
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... et al. 2008). For example, one strain (CPUml) retains the entire gene set involved in cysteine synthesis (i.e., cysE and cysK), but one or both these have been lost or occur as putative pseudogenes in the other nine strains (fig. 3). The phylogeny of C. punctulatus suggests that the cysE gene was lost or pseudogenized independently three times (fig. ...
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... independently underwent erosion in the lineages leading to extant Cryptocercus and Mastotermes. Among Cryptocercus strains, Blattabacterium genome erosion was gradual, and comparison of gene loss events with previous chronograms estimated for Cryptocercus ( Che et al. 2016) indicates that these events took place sequentially over the last 60 My (fig. 4). We also found evidence of further gene loss during the last 5 My in the Blattabacterium genome of the C. punctulatus species complex (CPU strains). In the earliest branching C. punctulatus lineage, Blattabacterium CPUml possesses functional cysE and cysK, and is presumably able to synthesize cysteine. In contrast, three other lineages ...
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... Aside from those in the Hemiptera, cockroaches are some of the best-studied invertebrates in the context of endosymbiosis. Unique to the group is Blattabacterium cuenoti (hereafter Blattabacterium), found in almost all species apart from the cave-adapted family Nocticolidae and all termites except Mastotermes darwiniensis (Lo et al., 2007;Kinjo et al., 2018;Evangelista et al., 2019). Blattabacterium occurs in fat body tissue-analogous to the vertebrate liver-and is transmitted transovarially, playing a role in provisioning nutrients to hosts from nitrogenous wastes, such as urea and ammonia (Brooks & Richards, 1955;Brooks, 1970;Sabree et al., 2009). ...
... Blattabacterium occurs in fat body tissue-analogous to the vertebrate liver-and is transmitted transovarially, playing a role in provisioning nutrients to hosts from nitrogenous wastes, such as urea and ammonia (Brooks & Richards, 1955;Brooks, 1970;Sabree et al., 2009). As it is strictly vertically transmitted, the phylogeny of Blattabacterium accurately recapitulates the ∼200 million years (My) of the evolutionary history of cockroaches (Kinjo et al., 2018;Evangelista et al., 2019;Beasley-Hall et al., 2021;Kinjo et al., 2021). ...
... DNA extractions of fat body tissue from 100% ethanol preserved cockroach specimens were performed using a QIAGEN DNeasy Blood and Tissue Kit. DNA sequencing was outsourced to Macrogen (Seoul, South Korea) or performed in-house at the Okinawa Institute of Science & Technology Graduate University using Illumina shotgun-sequencing technology, following the methods of Kinjo et al. (2018). Outgroup sequence data were obtained from GenBank, representing strains from other subfamilies within the Blaberidae (Table S2). ...
Microbial symbioses have had profound impacts on the evolution of animals. Conversely, changes in host biology may impact the evolutionary trajectory of symbionts themselves. Blattabacterium cuenoti is present in almost all cockroach species and enables hosts to subsist on a nutrient‐poor diet. To investigate if host biology has impacted Blattabacterium at the genomic level, we sequenced and analyzed 25 genomes from Australian soil‐burrowing cockroaches (Blaberidae: Panesthiinae), which have undergone at least seven separate subterranean, subsocial transitions from above‐ground, wood‐feeding ancestors. We find at least three independent instances of genome erosion have occurred in Blattabacterium strains exclusive to Australian soil‐burrowing cockroaches. These shrinkages have involved the repeated inactivation of genes involved in amino acid biosynthesis and nitrogen recycling, the core role of Blattabacterium in the host‐symbiont relationship. The most drastic of these erosions have occurred in hosts thought to have transitioned underground the earliest relative to other lineages, further suggestive of a link between gene loss in Blattabacterium and the burrowing behavior of hosts. As Blattabacterium is unable to fulfill its core function in certain host lineages, these findings suggest soil‐burrowing cockroaches must acquire these nutrients from novel sources. Our study represents one of the first cases, to our knowledge, of parallel host adaptations leading to concomitant parallelism in their mutualistic symbionts, further underscoring the intimate relationship between these two partners.
... Together, the similarly reduced genomes, the large shared gene fraction, and the perfect genome synteny across P. siddallii strains provide strong evidence for an evolutionary history marked by an early and rapid genome reduction followed by diversification with their leech hosts. This genome reduction, followed by host-symbiont codivergence and large-scale genome synteny, mirrors well-known examples of "ancient" nutritional symbionts of aphids (Tamas et al. 2002;Chong et al. 2019), Camponotus ants (Williams and Wernegreen 2015), cockroaches, and termites (Kinjo et al. 2018), among many others. ...
Strict blood-feeding animals are confronted with a strong B vitamin de_ciency. Blood-feeding leeches from the Glossiphoniidae family, similarly to haematophagous insects, have evolved specialised organs called bacteriomes to harbour symbiotic bacteria. Leeches of the Haementeria genus have two pairs of globular bacteriomes attached to the oesophagus which house intracellular 'Candidatus Providencia siddallii' bacteria. Previous work analysing a draft genome of the Providencia symbiont of the Mexican leech Haementeria officinalis showed that, in this species, the bacteria hold a reduced genome capable of synthesising B vitamins. In this work, we aimed to expand our knowledge on the diversity and evolution of Providencia symbionts of Haementeria. For this purpose, we sequenced the symbiont genomes of three selected leech species. We found that all genomes are highly syntenic and have kept a stable genetic repertoire, mirroring ancient insect endosymbionts. Additionally, we found B vitamin pathways to be conserved among these symbionts, pointing to a conserved symbiotic role. Lastly and most notably, we found that the symbiont of Haementeria acuecueyetzin has evolved an alternative genetic code, affecting a portion of its proteome and showing evidence of a lineage-specific and likely intermediate stage of genetic code reassignment.
... Together, the similarly-reduced genomes, the large shared gene fraction, and the perfect genome synteny across P. siddallii strains provide strong evidence for an evolutionary history marked by an early and rapid genome reduction followed by diversification with their leech hosts. This genome reduction followed by host-symbiont co-divergence mirrors well-known examples of "ancient" nutritional symbionts of aphids (Chong et al., 2019;Tamas et al., 2002), Camponotus ants (Williams and Wernegreen, 2015), cockroaches, and termites (Kinjo et al., 2018), among many others. ...
Strict blood-feeding animals are confronted with a strong B vitamin deficiency. Leeches from the Glossiphoniidae family, notably species of Placobdella, Placobdelloides, and Haementeria are regarded as strict blood-feeders, and similarly to blood-feeding insects, have evolved specialised organs called bacteriomes to harbour symbiotic bacteria. Leeches of the Haementeria genus are found exclusively in the Americas, with most species being South-American and only three found in North America. In these leeches, two pairs of globular bacteriomes attached to the oesophagus harbour intracellularly 'Candidatus Providencia siddallii' bacteria. Previous work analysing a draft genome of the Providencia symbiont of the Mexican leech Haementeria officinalis showed that, in this species, the bacteria hold a reduced genome with complete biosynthetic pathways for B vitamins. In this work, we aimed to expand our knowledge on the diversity and evolution of Providencia symbionts of Haementeria species. For this purpose, we sequenced the genomes of the Providencia symbionts of the Mexican leeches Haementeria acuecueyetzin and Haementeria lopezi, as well as re-sequenced and closed the symbiont genome of H. officinalis. We found that all genomes are highly syntenic, mirroring ancient insect endosymbionts and suggesting a conserved gene order at the start of the Providencia-Haementeria association. Additionally, we found B vitamin pathways to be conserved among these symbionts, pointing to a common biosynthetic machinery and low variation in this trait. Lastly and most notably, we found that the symbiont of H. acuecueyetzin has evolved an alternative genetic code, affecting a portion of its proteome and showing evidence of a rather recent and likely intermediate stage of genetic code reassignment.
... Blattabacterium CPUbr and MADAR have undergone further genome reduction, being ;50kbp smaller than other strains (28,29). The additional genome reduction in these strains is mostly due to the loss of many genes involved in EAA biosynthesis. ...
... The additional genome reduction in these strains is mostly due to the loss of many genes involved in EAA biosynthesis. It has been hypothesized that the loss of these genes occurred as a result of relaxed selection due to the provision of EAAs either by the gut symbiotic system established in the common ancestor of C. punctulatus and M. darwiniensis (28)(29)(30)(31), and/or through social transfer of nutrients (proctodeal trophallaxis). One of these gene losses is present as a single gap in the arginine biosynthetic pathway, and consists of the loss of the gene encoding the enzyme involved in the final step of arginine biosynthesis, ArgH (EC 4.3.2.1). ...
... Although the products of the two Blattabacterium genes purB and fumC possibly replace the function of ArgH (30), the host genome also encodes arginosuccinate lyase (ASL: EC 4.3.2.1), an enzyme with a catalytic function similar to ArgH. The loss of ArgH has occurred in parallel in the ancestors of CPUbr and MADAR (29). A collaborative pathway involving the loss of ArgH by the endosymbiont Carsonella and complementation by a psyllid host gene was reported by Sloan et al. (2014), based on transcriptomic evidence. ...
The long-term coevolution between insects and their obligate endosymbionts is accompanied by increasing levels of genome integration, sometimes to the point that metabolic pathways require enzymes encoded in two genomes, which we refer to as “collaborative pathways”. To date, collaborative pathways have only been reported from sap-feeding insects.
... The acquisition of Blattabacterium took place in a common ancestor of cockroaches and termites [74,75]. However, termites have lost Blattabacterium, with the single exception of the xylophagous lower termite M. darwiniensis [76,77], which has preserved the endosymbiont, but with a reduced genome, similar to that of Cryptocercus [67,74,78]. Key events in the evolution from the common ancestor of termites and Cryptoceridae allowed the shift from an omnivorous to a cellulose-based diet [79]. ...
Mutualistic stable symbioses are widespread in all groups of eukaryotes, especially in insects, where symbionts have played an essential role in their evolution. Many insects live in obligate relationship with different ecto- and endosymbiotic bacteria, which are needed to maintain their hosts’ fitness in their natural environment, to the point of even relying on them for survival. The case of cockroaches (Blattodea) is paradigmatic, as both symbiotic systems coexist in the same organism in two separated compartments: an intracellular endosymbiont (Blattabacterium) inside bacteriocytes located in the fat body, and a rich and complex microbiota in the hindgut. The German cockroach Blattella germanica is a good model for the study of symbiotic interactions, as it can be maintained in the laboratory in controlled populations, allowing the perturbations of the two symbiotic systems in order to study the communication and integration of the tripartite organization of the host–endosymbiont–microbiota, and to evaluate the role of symbiotic antimicrobial peptides (AMPs) in host control over their symbionts. The importance of cockroaches as reservoirs and transmission vectors of antibiotic resistance sequences, and their putative interest to search for AMPs to deal with the problem, is also discussed.
... Mastotermes darwiniensis is the only lower termite that retains the endosymbiont B. cuenoti. However, compared with B. cuenoti in cockroaches, the genome of B. cuenoti in M. darwiniensis is sharp reduced, so it is speculated that uric acid degradation in M. darwiniensis should be co-mediated by B. cuenoti and hindgut symbionts [63,64]. Uricolytic strains, such as Clostridia, Enterobacteriaceae, also widely exist in the guts of Reticulitermes speratus, Coptotermes formosanus, Neotermes koshunensis, Glyptotermes fuscus, Cryptotermes domesticus, Hodotermopsis sjoestedti, O. formosanus, and Nasutitermes takasagoensis. ...
Nitrogen is usually a restrictive nutrient that affects the growth and development of insects, especially of those living in low nitrogen nutrient niches. In response to the low nitrogen stress, insects have gradually developed symbiont-based stress response strategies—biological nitrogen fixation and nitrogenous waste recycling—to optimize dietary nitrogen intake. Based on the above two patterns, atmospheric nitrogen or nitrogenous waste (e.g., uric acid, urea) is converted into ammonia, which in turn is incorporated into the organism via the glutamine synthetase and glutamate synthase pathways. This review summarized the reaction mechanisms, conventional research methods and the various applications of biological nitrogen fixation and nitrogenous waste recycling strategies. Further, we compared the bio-reaction characteristics and conditions of two strategies, then proposed a model for nitrogen provisioning based on different strategies.
... Our results support the monophyly of Cryptocercus and termites, and the sister group relationship between Asian and North American Cryptocercus, in line with a recent mitochondrial genome phylogeny . In the North American clade, our results almost concur with the results of Kinjo et al. (2018) based on Blattabacterium genomes. The phylograms (Fig. 4, S1-S3) based on different datasets (RNAPCG12 or RNAPCG12tRNA) using Bayesian inference and maximum-likelihood recovered the monophyly of C. clevelandi and the C. punctulatus complex (Kinjo et al., 2018). ...
... In the North American clade, our results almost concur with the results of Kinjo et al. (2018) based on Blattabacterium genomes. The phylograms (Fig. 4, S1-S3) based on different datasets (RNAPCG12 or RNAPCG12tRNA) using Bayesian inference and maximum-likelihood recovered the monophyly of C. clevelandi and the C. punctulatus complex (Kinjo et al., 2018). Relationships among members of the C. punctulatus complex were partly inconsistent with the result of Che et al. (2016), which might be the result of using different types of data and different taxon sampling. ...
Cryptocercus Scudder, a genus of wingless, subsocial cockroaches, has low vagility but exhibits a disjunct distribution in eastern and western North America, and in China, South Korea and the Russian Far East. This distribution provides an ideal model for testing hypotheses of vicariance through plate tectonics or other natural barriers versus transoceanic dispersal or across other natural barriers. We sequenced 45 Cryptocercus mitochondrial genomes to resolve phylogenetic relationships among members of the genus worldwide. We identified four types of tRNAs rearrangements among samples from the Qin-Daba Mountains. Our maximum-likelihood and Bayesian phylogenetic trees, based on mitochondrial genomes and nuclear genes (18S, 28S), strongly supported six major lineages of Cryptocercus, which displayed a clear geographical distribution pattern. We used Bayesian molecular dating to estimate the evolutionary timescale of the genus, and reconstructed Cryptocercus ancestral ranges using statistical dispersal-vicariance analysis (S-DIVA) in RASP. Two dispersal events and six vicariance events for Cryptocercus were inferred with high support. The initial vicariance event occurred between American and Asian lineages at 80.5 Ma (95% credibility interval: 60.0-104.7 Ma), followed by one vicariance event within the American lineage 43.8 Ma (95% CI: 32.0-57.5 Ma), and two dispersal 31.9 Ma (95% CI: 25.8-39.5 Ma), 21.7 Ma (95% CI: 17.3-27.1 Ma) plus four vicariance events c. 29.3 Ma, 27.2 Ma, 24.8 Ma and 16.7 Ma within the Asian lineage. Our analyses provide evidence that both vicariance and dispersal have played important roles in shaping the distribution and diversity of these woodroaches.
... The largest genomes of Blattabacterium are 630 À 640 kb. Several lineages independently experienced further reduction and have genomes as small as 511 kb (L opez-S anchez et al. 2009;Sabree et al. 2009;Neef et al. 2011;Huang et al. 2012;Sabree et al. 2012;Kambhampati et al. 2013;Patiño-Navarrete et al. 2013;Tokuda et al. 2013;Kinjo et al. 2015Kinjo et al. , 2018Vicente et al. 2018;Bourguignon et al. 2020). For example, the sister strains of Blattabacterium associated with the woodroach Cryptocercus punctulatus and M. darwiniensis have reduced genomes of 610 and 590 kb, respectively, and have experienced independent genome reduction, as indicated by the relatively large 637 kb genome of the strain of Cryptocercus kyebangensis (Kinjo et al. 2018). ...
... Several lineages independently experienced further reduction and have genomes as small as 511 kb (L opez-S anchez et al. 2009;Sabree et al. 2009;Neef et al. 2011;Huang et al. 2012;Sabree et al. 2012;Kambhampati et al. 2013;Patiño-Navarrete et al. 2013;Tokuda et al. 2013;Kinjo et al. 2015Kinjo et al. , 2018Vicente et al. 2018;Bourguignon et al. 2020). For example, the sister strains of Blattabacterium associated with the woodroach Cryptocercus punctulatus and M. darwiniensis have reduced genomes of 610 and 590 kb, respectively, and have experienced independent genome reduction, as indicated by the relatively large 637 kb genome of the strain of Cryptocercus kyebangensis (Kinjo et al. 2018). Interestingly, many genes involved in amino acid biosynthesis were lost in parallel in both strains (Kinjo et al. 2018), possibly compensated by the stable association their host established with their largely vertically transmitted gut microbes (Brune 2014). ...
... For example, the sister strains of Blattabacterium associated with the woodroach Cryptocercus punctulatus and M. darwiniensis have reduced genomes of 610 and 590 kb, respectively, and have experienced independent genome reduction, as indicated by the relatively large 637 kb genome of the strain of Cryptocercus kyebangensis (Kinjo et al. 2018). Interestingly, many genes involved in amino acid biosynthesis were lost in parallel in both strains (Kinjo et al. 2018), possibly compensated by the stable association their host established with their largely vertically transmitted gut microbes (Brune 2014). How common parallel gene loss is in Blattabacterium remains to be understood. ...
Intracellular endosymbionts have reduced genomes that progressively lose genes at a timescale of tens of million years. We previously reported that gene loss rate is linked to mutation rate in Blattabacterium, however, the mechanisms causing gene loss are not yet fully understood. Here, we carried out comparative genomic analyses on the complete genome sequences of a representative set of 67 Blattabacterium strains, with sizes ranging between 511kbp and 645kbp. We found that 200 of the 566 analysed protein-coding genes were lost in at least one lineage of Blattabacterium, with the most extreme case being one gene that was lost independently in 24 lineages. We found evidence for three mechanisms influencing gene loss in Blattabacterium. First, gene loss rates were found to increase exponentially with the accumulation of substitutions. Second, genes involved in vitamin and amino acid metabolism experienced relaxed selection in Cryptocercus and Mastotermes, possibly triggered by their vertically-inherited gut symbionts. Third, we found evidences of epistatic interactions among genes leading to a ‘domino effect’ of gene loss within pathways. Our results highlight the complexity of the process of genome erosion in an endosymbiont.
... Blattabacterium Hollande & Favre is a strictly vertically transmitted, intracellular mutualist present in the fat body of almost all cockroaches, and this relationship is thought to have existed for over 150 million years Evangelista et al., 2019). The phylogeny of this bacterium is known to be highly concerted with that of its hosts, and provides an ideal additional locus with which to infer host evolutionary relationships Maekawa et al., 2005;Kinjo et al., 2018;Arab et al., 2020). In this study, we specifically aim to investigate: (i) how many times soil-burrowing behaviour and associated fossorial morphology have evolved in parallel within Geoscapheinae and Panesthiinae, including clarifying the phylogenetic position of P. sloanei, P. australis, P. obtusa, P. tryoni ssp. ...
Soil‐burrowing cockroaches (Blaberidae: Geoscapheinae) are large insects endemic to Australia. Originally thought to represent a monophyletic group, these enigmatic species have in fact evolved burrowing behaviour, associated fossorial morphological modifications, and dietary transitions to dry leaf litter feeding multiple times from the wood‐feeding Panesthiinae in a striking example of parallel evolution. However, various relationships within these two subfamilies remain unresolved or poorly understood, notably the apparent paraphyly of Panesthiinae with respect to Geoscapheinae, the position and diversification of certain species within major clades, and several aspects of the overall group's biogeography and morphological evolution. Here, we investigate the phylogeny of Australian members of these two subfamilies using whole mitochondrial genomes paired with nuclear ribosomal markers and highly conserved genes from the bacterial endosymbiont Blattabacterium. Using the resulting robust, fossil‐calibrated phylogeny from these three sources we confirm the nonmonophyly of both subfamilies and recover Geoscapheinae as polyphyletic within a paraphyletic Panesthiinae. The nonmonophyly of natural groups, at all levels from subfamily to species, has been driven by repeated, independent acquisitions of burrowing forms in Geoscapheinae from panesthiine ancestors that colonized the continent on two separate occasions during the Miocene. We additionally find morphological variation within Geoscapheinae itself is correlated with species distributions. Older soil‐burrowing clades living in comparatively arid environments have additional morphological reductions beyond obvious fossorial adaptations compared to those in younger burrowing clades from more temperate habitats. Ultimately, the results presented here demonstrate connections among phylogeny, biogeography and morphology throughout Australian representatives of these two subfamilies, factors that could not be previously consolidated using existing phylogenetic frameworks. Given the discordance between molecular data implemented here and the existing taxonomic classification, we find no support for retaining Geoscapheinae as a discrete taxonomic grouping. In closing, we discuss the taxonomic implications of these results and present a roadmap for future research on Geoscapheinae and their panesthiine relatives.
... Genome-wide analyses of the symbiont have indicated that it plays a role in host nitrogen metabolism and the synthesis of essential amino acids [16,17]. The genomes of 21 Blattabacterium strains sequenced to date are highly reduced compared with those of their free-living relatives, ranging in size from 590 to 645 kb [16][17][18][19][20]. They contain genes encoding enzymes for DNA replication and repair, with some exceptions (holA, holB and mutH) [16][17][18][19][20]. ...
... The genomes of 21 Blattabacterium strains sequenced to date are highly reduced compared with those of their free-living relatives, ranging in size from 590 to 645 kb [16][17][18][19][20]. They contain genes encoding enzymes for DNA replication and repair, with some exceptions (holA, holB and mutH) [16][17][18][19][20]. The extent to which host nuclear proteins are involved in the cell biology of Blattabacterium, and particularly DNA replication, is not well understood. ...
Bacterial endosymbionts evolve under strong host-driven selection. Factors influencing host evolution might affect symbionts in similar ways, potentially leading to correlations between the molecular evolutionary rates of hosts and symbionts. Although there is evidence of rate correlations between mitochondrial and nuclear genes, similar investigations of hosts and sym-bionts are lacking. Here, we demonstrate a correlation in molecular rates between the genomes of an endosymbiont (Blattabacterium cuenoti) and the mitochondrial genomes of their hosts (cockroaches). We used partial genome data for multiple strains of B. cuenoti to compare phylogenetic relationships and evolutionary rates for 55 cockroach/symbiont pairs. The phylogenies inferred for B. cuenoti and the mitochondrial genomes of their hosts were largely congruent, as expected from their identical maternal and cytoplasmic mode of inheritance. We found a correlation between evolutionary rates of the two genomes, based on comparisons of root-to-tip distances and on comparisons of the branch lengths of phylogenetically independent species pairs. Our results underscore the profound effects that long-term symbiosis can have on the biology of each symbiotic partner.
