Complete Genome Sequence of “Candidatus Sulcia muelleri” ML, an Obligate Nutritional Symbiont of Maize Leafhopper (
            <i>Dalbulus maidis</i>
            )

Chang, Hsing-Hua; Cho, Shu-Ting; Canale, Maria Cristina; Mugford, Sam T.; Lopes, J. R. S.; Hogenhout, Saskia A.; Kuo, Chih-Horng

doi:10.1128/genomea.01483-14

Cited by 23 publications

(22 citation statements)

References 26 publications

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“…Similarly, both Sulcia -ALF and Sulcia -ENCA have lost many genes involved in the formation of major oxidative phosphorylation (OXPHOS) protein complexes, including cytochrome C oxidase and NADH dehydrogenase. Although, both lineages do retain the subunits required for ATP synthase formation and is also conserved in all other sequenced Sulcia genomes ( McCutcheon and Moran 2010 ; Koga and Moran 2014 ; Van Leuven et al 2014 ; Chang et al 2015 ). We were further able to identify a truncated gene fragment for the Cbb3-type cytochrome c oxidase subunit III ( ccoP ), which is ∼10% (105 bp) of its predicted length in E. coli .…”

Section: Resultsmentioning

confidence: 99%

“…5 B ). The incomplete set of the tRNA synthetases is commonly found in the Sulcia genomes, while the number of genes retained is variable among different lineages ( Wu et al 2006 ; McCutcheon and Moran 2007 ; McCutcheon et al 2009 ; McCutcheon and Moran 2010 ; Bennett and Moran 2013 ; Bennett et al 2014 ; Chang et al 2015 ). It is notable that Sulcia -ENCA has the same tRNA synthetases as found in some lineages from xylem-feeding sharpshooter leafhoppers (Cicadellinae) ( McCutcheon and Moran 2007 ).…”

Section: Resultsmentioning

confidence: 99%

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Comparative Genomics of the Dual-Obligate Symbionts from the Treehopper, Entylia carinata (Hemiptera: Membracidae), Provide Insight into the Origins and Evolution of an Ancient Symbiosis

Mao

Yang

Poff

et al. 2017

Genome Biology and Evolution

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Insect species in the Auchenorrhyncha suborder (Hemiptera) maintain ancient obligate symbioses with bacteria that provide essential amino acids (EAAs) deficient in their plant-sap diets. Molecular studies have revealed that two complementary symbiont lineages, “Candidatus Sulcia muelleri” and a betaproteobacterium (“Ca. Zinderia insecticola” in spittlebugs [Cercopoidea] and “Ca. Nasuia deltocephalinicola” in leafhoppers [Cicadellidae]) may have persisted in the suborder since its origin ∼300 Ma. However, investigation of how this pair has co-evolved on a genomic level is limited to only a few host lineages. We sequenced the complete genomes of Sulcia and a betaproteobacterium from the treehopper, Entylia carinata (Membracidae: ENCA), as the first representative from this species-rich group. It also offers the opportunity to compare symbiont evolution across a major insect group, the Membracoidea (leafhoppers + treehoppers). Genomic analyses show that the betaproteobacteria in ENCA is a member of the Nasuia lineage. Both symbionts have larger genomes (Sulcia = 218 kb and Nasuia = 144 kb) than related lineages in Deltocephalinae leafhoppers, retaining genes involved in basic cellular functions and information processing. Nasuia-ENCA further exhibits few unique gene losses, suggesting that its parent lineage in the common ancestor to the Membracoidea was already highly reduced. Sulcia-ENCA has lost the abilities to synthesize menaquinone cofactor and to complete the synthesis of the branched-chain EAAs. Both capabilities are conserved in other Sulcia lineages sequenced from across the Auchenorrhyncha. Finally, metagenomic sequencing recovered the partial genome of an Arsenophonus symbiont, although it infects only 20% of individuals indicating a facultative role.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Comparative Genomics of the Dual-Obligate Symbionts from the Treehopper, Entylia carinata (Hemiptera: Membracidae), Provide Insight into the Origins and Evolution of an Ancient Symbiosis

Mao

Yang

Poff

et al. 2017

Genome Biology and Evolution

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“…3). Sulcia-OLIH is the smallest Sulcia strain yet sequenced and has lost approximately 40 kb (38 genes) compared with Sulcia from Deltocephalinae leafhoppers (Bennett et al, 2016a;Chang et al, 2015;Bennett and Moran, 2013). Gene losses are widespread among functional categories, including all energy synthesis genes (e.g., atpABCDEFGH, gapA and sucAB), transcription and translation (rpsT, rpmE, rsmI and trmH), protein transport and degradation (secAY and lepB), and various essential intermediate metabolites such as pyruvate and succinyl-CoA (korAB and sucABCD) ( Fig.…”

Section: Figmentioning

confidence: 99%

“…The Cicadomorpha and Fulgoroidea likely split early in the diversification of the Auchenorrhyncha (~250 MYA; Shcherbakov, 2002;Szwedo et al, 2004). Although no genomic examples currently exist for a planthopper symbiosis, comparative analyses of Sulcia genomes from the Cicadomorpha reveal that it plays a central role in the symbiosis, provisioning 7 or 8 of the 10 EAAs required by its hosts (Wu et al, 2006;McCutcheon and Moran, 2010;Bennett and Moran, 2013;Koga and Moran, 2014;Chang et al, 2015). Its partner symbionts synthesize the remaining EAAs.…”

Section: Introductionmentioning

confidence: 99%

Comparative genomics of a quadripartite symbiosis in a planthopper host reveals the origins and rearranged nutritional responsibilities of anciently diverged bacterial lineages

Bennett

Mao

2018

Environmental Microbiology

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Insects in the Auchenorrhyncha (Hemiptera: Suborder) established nutritional symbioses with bacteria approximately 300 million years ago (MYA). The suborder split early during its diversification (~ 250 MYA) into the Fulgoroidea (planthoppers) and Cicadomorpha (leafhoppers and cicadas). The two lineages share some symbionts, including Sulcia and possibly a Betaproteobacteria that collaboratively provide their hosts with 10 essential amino acids (EAA). Some hosts harbour three bacteria, as is common among planthoppers. However, genomic studies are currently restricted to the dual-bacterial symbioses found in Cicadomorpha, leaving the origins and functions of these more complex symbioses unclear. To address these questions, we sequenced the genomes and performed phylogenomic analyses of 'Candidatus Sulcia muelleri' (Bacteroidetes), 'Ca. Vidania fulgoroideae' (Betaproteobacteria) and 'Ca. Purcelliella pentastirinorum' (Gammaproteobacteria) from a planthopper (Cixiidae: Oliarus). In contrast to the Cicadomorpha, nutritional synthesis responsibilities are rearranged between the cixiid symbionts. Although Sulcia has a highly conserved genome across the Auchenorrhyncha, in the cixiids it is greatly reduced and provides only three EAAs. Vidania contributes the remaining seven EAAs. Phylogenomic results suggest that it represents an ancient symbiont lineage paired with Sulcia throughout the Auchenorrhyncha. Finally, Purcelliella was recently acquired from plant-insect associated bacteria (Pantoea-Erwinia) to provide B vitamins and metabolic support to its degenerate partners.

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“…Rather, we hypothesize that these sorted-MAGs have an alternative survival strategy in the soil environment similar to those exhibited by other Bacteroidetes, including "Candidatus Amoebophilus asiaticus" (84), Cardinium sp. (85), "Candidatus Sulcia muelleri" (86), and Blattabacterium sp. (87), which are known symbionts (Fig.…”

Section: Resultsmentioning

confidence: 99%

Complementary Metagenomic Approaches Improve Reconstruction of Microbial Diversity in a Forest Soil

et al. 2020

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Soil ecosystems harbor diverse microorganisms and yet remain only partially characterized as neither single-cell sequencing nor whole-community sequencing offers a complete picture of these complex communities. Thus, the genetic and metabolic potential of this "uncultivated majority" remains underexplored. To address these challenges, we applied a pooled-cell-sorting-based mini-metagenomics approach and compared the results to bulk metagenomics. Informatic binning of these data produced 200 mini-metagenome assembled genomes (sorted-MAGs) and 29 bulk metagenome assembled genomes (MAGs). The sorted and bulk MAGs increased the known phylogenetic diversity of soil taxa by 7.2% with respect to the Joint Genome Institute IMG/M database and showed clade-specific sequence recruitment patterns across diverse terrestrial soil metagenomes. Additionally, sorted-MAGs expanded the rare biosphere not captured through MAGs from bulk sequences, exemplified through phylogenetic and functional analyses of members of the phylum Bacteroidetes. Analysis of 67 Bacteroidetes sorted-MAGs showed conserved patterns of carbon metabolism across four clades. These results indicate that mini-metagenomics enables genomeresolved investigation of predicted metabolism and demonstrates the utility of combining metagenomics methods to tap into the diversity of heterogeneous microbial assemblages. IMPORTANCE Microbial ecologists have historically used cultivation-based approaches as well as amplicon sequencing and shotgun metagenomics to characterize microbial diversity in soil. However, challenges persist in the study of microbial diversity, including the recalcitrance of the majority of microorganisms to laboratory cultivation and limited sequence assembly from highly complex samples. The uncultivated majority thus remains a reservoir of untapped genetic diversity. To address some of the challenges associated with bulk metagenomics as well as low throughput of single-cell genomics, we applied flow cytometry-enabled mini-metagenomics to capture expanded microbial diversity from forest soil and compare it to soil bulk metagenomics. Our resulting data from this pooled-cell sorting approach combined with bulk metagenomics revealed increased phylogenetic diversity through novel soil taxa and rare biosphere members. In-depth analysis of genomes within the highly represented Bacteroidetes phylum provided insights into conserved and cladespecific patterns of carbon metabolism.

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Complete Genome Sequence of “Candidatus Sulcia muelleri” ML, an Obligate Nutritional Symbiont of Maize Leafhopper ( Dalbulus maidis )

Cited by 23 publications

References 26 publications

Comparative Genomics of the Dual-Obligate Symbionts from the Treehopper, Entylia carinata (Hemiptera: Membracidae), Provide Insight into the Origins and Evolution of an Ancient Symbiosis

Comparative Genomics of the Dual-Obligate Symbionts from the Treehopper, Entylia carinata (Hemiptera: Membracidae), Provide Insight into the Origins and Evolution of an Ancient Symbiosis

Comparative genomics of a quadripartite symbiosis in a planthopper host reveals the origins and rearranged nutritional responsibilities of anciently diverged bacterial lineages

Complementary Metagenomic Approaches Improve Reconstruction of Microbial Diversity in a Forest Soil

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