Cladogenesis and Genomic Streamlining in Extracellular Endosymbionts of Tropical Stink Bugs

Otero-Bravo, Alejandro; Goffredi, Shana K.; Sabree, Zakee L.

doi:10.1093/gbe/evy033

Cited by 22 publications

(24 citation statements)

References 78 publications

(89 reference statements)

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“…Organismal scope or featured taxon Cunha & Giribet (2019) yes Gastropods Laumer et al (2019) yes Animals Lemer et al (2019) yes Bivalves Lozano-Fernandez et al (2019) yes Chelicerates Marlétaz et al (2019) yes Spiralia Philippe et al (2019) yes Bilateria Narayanan Kutty et al (2019) no Calyptratae Uribe et al (2019) no Gastropods Wolfe et al (2019) no Decapod crustaceans Zverkov et al (2019) no Dicyemida and Orthonectida Aouad et al (2018) yes Archaea Laumer et al (2018) yes Placozoa Otero-Bravo et al (2018) yes Pantoea Puttick et al (2018) yes Land plants Schwentner et al (2018) yes Pancrustacea Sousa et al (2018) yes Land plants Bennett & Mao (2018) no Fulgoroidea symbionts Eitel et al (2018) no Placozoa Manzano-Marín et al (2018) no Cinara strobi symbionts Feuda et al (2017) yes Animals Szabó et al (2017) yes Pseudococcidae symbionts Williams et al (2017) yes Archaea Schwentner et al (2017) no Pancrustacea Shin et al (2017) no Curculionoidea Simion et al (2017) no Animals Yoshida et al (2017) no Tardigrades Leliaert et al (2016) yes Viridiplantae Zhang et al (2016) yes Roseobacter CHAB-I-5 lineage He et al (2016) no Rhizaria Song et al (2016) no Holometabola Domman et al (2015) yes Plastids Luo (2015) yes SAR11 Petitjean et al (2015) yes Archaea Borowiec et al (2015) no Animals Derelle et al (2015) no Eukaryotes Wang & Wu (2015) no Mitochondria…”

Section: Citationmentioning

confidence: 99%

Six-state amino acid recoding is not an effective strategy to offset the effects of compositional heterogeneity and saturation in phylogenetic analyses

Hernandez

Ryan

2019

Preprint

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Six-state amino acid recoding strategies are commonly applied to combat the effects of compositional heterogeneity and substitution saturation in phylogenetic analyses. While these methods have been endorsed from a theoretical perspective, their performance has never been extensively tested. Here, we test the effectiveness of 6-state recoding approaches by comparing the performance of analyses on recoded and non-recoded datasets that have been simulated under gradients of compositional heterogeneity or saturation. In all of our simulation analyses, non-recoding approaches greatly outperformed 6-state recoding approaches. Our results suggest that 6-state recoding strategies are not effective in the face of high saturation. Further, while recoding strategies do buffer the effects of compositional heterogeneity, the loss of information that accompanies 6-state recoding outweighs its benefits, even in the most compositionally heterogeneous datasets. In addition, we evaluate recoding schemes with 9, 12, 15, and 18 states and show that these all outperform 6-state recoding. Our results have important implications for the more than 70 published papers that have incorporated 6-state recoding, many of which have significant bearing on relationships across the tree of life.

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Section: Citationmentioning

confidence: 99%

Six-state amino acid recoding is not an effective strategy to offset the effects of compositional heterogeneity and saturation in phylogenetic analyses

Hernandez

Ryan

2019

Preprint

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“…The almost full‐length gene sequences (1463 bp; MG725752.1) were identical, with best blast hits with different Pantoea species (up to 99.04% identity). This initial result suggested the affiliation to the Pantoea genus, consistently with findings in other Pentatomidae species (Kenyon et al ., 2015; Duron and Noël, 2016; Hosokawa et al ., 2016a; Hosokawa et al ., 2016b; Otero‐Bravo et al ., 2018).…”

Section: Resultsmentioning

confidence: 99%

“…This region, referred to as V4 or M4, contains specialized invaginations or ‘crypts’ to house symbionts (Buchner, 1965; Gordon et al ., 2016; Hosokawa et al ., 2016a; Hosokawa et al ., 2016b; Karamipour et al ., 2016; Kashkouli et al ., 2019a; Kashkouli et al ., 2019b, 2020). These extracellular symbionts differ in their transmission routes from bacteriocyte‐associated ones, as at each generation the offspring must acquire them via consumption of symbiont‐laden gut secretions deposited on the egg surfaces by the mother (Kikuchi et al ., 2009; Prado and Almeida, 2009; Salem et al ., 2014; Otero‐Bravo et al ., 2018). While this pattern is shared by pentatomoidean bugs of different families, some lineage‐specific features exist.…”

Section: Introductionmentioning

confidence: 99%

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Characterization of a novel Pantoea symbiont allows inference of a pattern of convergent genome reduction in bacteria associated with Pentatomidae

Kashkouli

Castelli

Floriano

et al. 2020

Environmental Microbiology

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Summary Phytophagous stink bugs typically harbor nutritional symbiotic bacteria in their midgut, to integrate their unbalanced diet. In the Pentatomidae, most symbionts are affiliated to the genus Pantoea, and are polyphyletic. This suggests a scenario of an ancestral establishment of symbiosis, followed by multiple symbiont replacement events by akin environmental bacteria in different host lineages. In this study, a novel Pantoeaspecies (‘CandidatusPantoea persica’) was characterized from the gut of the pentatomid Acrosternum arabicum, and shown to be highly abundant in a specific portion of the gut and necessary for the host development. The genome of the symbiont (2.9 Mb), while presenting putative host‐supportive metabolic pathways, including those for amino acids and vitamin synthesis, showed a high level of pseudogenization, indicating ongoing genome reduction. Comparative analyses with other free‐living and symbiotic Pantoea highlighted a convergent pattern of genome reduction in symbionts of pentatomids, putatively following the typical phases modelized in obligate nutritional symbionts of insects. Additionally, this system has distinctive traits, as hosts are closely related, and symbionts originated multiple independent times from closely related free‐living bacteria, displaying convergent and independent conspicuous genome reduction. Due to such peculiarities, this may become an ideal model to study genome evolutionary processes in insect symbionts.

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“…Synechococcus spongiarum” is found extracellularly in the sponge host rather than in bacteriocytes. Extracellular, obligate, and vertically transmitted symbionts can be also found in insects (35), yet they are understudied compared to their intracellular counterparts. While genome-based studies of extracellular and (primarily) vertically transmitted sponge symbionts have occupied the focus of published studies, including the cyanobacterium “ Ca.…”

Section: Introductionmentioning

confidence: 99%

Life at Home and on the Roam: Genomic Adaptions Reflect the Dual Lifestyle of an Intracellular, Facultative Symbiont

et al. 2019

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“Candidatus Synechococcus feldmannii” is a facultative intracellular symbiont of the Atlanto-Mediterranean sponge Petrosia ficiformis. Genomic information of sponge-associated cyanobacteria derives thus far from the obligate and extracellular symbiont “Candidatus Synechococcus spongiarum.” Here we utilized a differential methylation-based approach for bacterial DNA enrichment combined with metagenomics to obtain the first draft genomes of “Ca. Synechococcus feldmannii.” By comparative genomics, we revealed that some genomic features (e.g., iron transport mediated by siderophores, eukaryotic-like proteins, and defense mechanisms, like CRISPR-Cas [clustered regularly interspaced short palindromic repeats-associated proteins]) are unique to both symbiont types and absent or rare in the genomes of taxonomically related free-living cyanobacteria. These genomic features likely enable life under the conditions found inside the sponge host. Interestingly, there are many genomic features that are shared by “Ca. Synechococcus feldmannii” and free-living cyanobacteria, while they are absent in the obligate symbiont “Ca. Synechococcus spongiarum.” These include genes related to cell surface structures, genetic regulation, and responses to environmental stress, as well as the composition of photosynthetic genes and DNA metabolism. We speculate that the presence of these genes confers on “Ca. Synechococcus feldmannii” its facultative nature (i.e., the ability to respond to a less stable environment when free-living). Our comparative analysis revealed that distinct genomic features depend on the nature of the symbiotic interaction: facultative and intracellular versus obligate and extracellular. IMPORTANCE Given the evolutionary position of sponges as one of the earliest phyla to depart from the metazoan stem lineage, studies on their distinct and exceptionally diverse microbial communities should yield a better understanding of the origin of animal-bacterium interactions. While genomes of several extracellular sponge symbionts have been published, the intracellular symbionts have, so far, been elusive. Here we compare the genomes of two unicellular cyanobacterial sponge symbionts that share an ancestor but followed different evolutionary paths—one became intracellular and the other extracellular. Counterintuitively, the intracellular cyanobacteria are facultative, while the extracellular ones are obligate. By sequencing the genomes of the intracellular cyanobacteria and comparing them to the genomes of the extracellular symbionts and related free-living cyanobacteria, we show how three different cyanobacterial lifestyles are reflected by adaptive genomic features.

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Cladogenesis and Genomic Streamlining in Extracellular Endosymbionts of Tropical Stink Bugs

Cited by 22 publications

References 78 publications

Six-state amino acid recoding is not an effective strategy to offset the effects of compositional heterogeneity and saturation in phylogenetic analyses

Six-state amino acid recoding is not an effective strategy to offset the effects of compositional heterogeneity and saturation in phylogenetic analyses

Characterization of a novel Pantoea symbiont allows inference of a pattern of convergent genome reduction in bacteria associated with Pentatomidae

Life at Home and on the Roam: Genomic Adaptions Reflect the Dual Lifestyle of an Intracellular, Facultative Symbiont

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