The Importance of Revisiting Legionellales Diversity

Duron, Olivier; Doublet, Patricia; Vavre, Fabrice; Bouchon, Didier

doi:10.1016/j.pt.2018.09.008

Cited by 28 publications

(27 citation statements)

References 77 publications

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“…A similar phenomenon was suggested for the detection of 16 novel giant viruses from these same samples (40), as these viruses are most often associated with eukaryotic host cells (59). The hypothesized liberation of these intracellular bacteria makes mini-metagenomic sequencing a useful tool for investigating the diversity and evolution of the intracellular life strategy (55,60).…”

Section: Resultssupporting

confidence: 54%

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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Section: Resultssupporting

confidence: 54%

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

et al. 2020

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“…The recent realization that human pathogens such as Chlamydiae, Legionellales and Rickettsiales have close relatives that live in hosts ranging from protists to fish and from aquatic and soil habitats has led to a paradigm shift in our view of the ecology and evolution of intracellular bacteria 27,39,40 . ‘ G. incantans ’ extends our conceptual understanding of the pervasiveness of such bacteria and shows that a single environmental rickettsial genus occurs worldwide in marine and limnic habitats.…”

Section: Mainmentioning

confidence: 99%

Two intracellular and cell type-specific bacterial symbionts in the placozoan Trichoplax H2

et al. 2019

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Placozoa is an enigmatic phylum of simple, microscopic, marine metazoans1,2. Although intracellular bacteria have been found in all members of this phylum, almost nothing is known about their identity, location and interactions with their host3–6. We used metagenomic and metatranscriptomic sequencing of single host individuals, plus metaproteomic and imaging analyses, to show that the placozoan Trichoplax sp. H2 lives in symbiosis with two intracellular bacteria. One symbiont forms an undescribed genus in the Midichloriaceae (Rickettsiales)7,8 and has a genomic repertoire similar to that of rickettsial parasites9,10, but does not seem to express key genes for energy parasitism. Correlative image analyses and three-dimensional electron tomography revealed that this symbiont resides in the rough endoplasmic reticulum of its host’s internal fibre cells. The second symbiont belongs to the Margulisbacteria, a phylum without cultured representatives and not known to form intracellular associations11–13. This symbiont lives in the ventral epithelial cells of Trichoplax, probably metabolizes algal lipids digested by its host and has the capacity to supplement the placozoan’s nutrition. Our study shows that one of the simplest animals has evolved highly specific and intimate associations with symbiotic, intracellular bacteria and highlights that symbioses can provide access to otherwise elusive microbial dark matter.

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“…The genus Legionella was first recognized in the late 1970s, with the characterization of Legionella pneumophila as the aetiological agent of a form of pneumonia now known as Legionnaires’ disease [1, 2]. Within the G amma proteobacteria , Legionella is the sole genus contained within the family Legionellaceae [3]. Members of this genus are Gram-negative bacteria found ubiquitously in the environment in both freshwater systems such as lakes and rivers, as well as man-made aquatic systems [4–7].…”

Section: Legionella Taxonomy and Pathogenesismentioning

confidence: 99%

“…Legionella species (the sole members of the family Legionellaceae ) are most closely related to members of the family Coxiellaceae which contains Coxiella , Rickettsiella , Aquicella, Berkiella, Occultobacter and Nucleophilum among others , which together with Legionellaceae make up the order Legionellales [3]. It was previously reported that Coxiella burnettii , although possessing a T4SS, lacks a core set of T2SS genes [50, 237].…”

Section: On the Origins Of The Legionella Lsp T2ssmentioning

confidence: 99%

Assessing the impact, genomics and evolution of type II secretion across a large, medically important genus: the Legionella type II secretion paradigm

White

Cianciotto

2019

Microbial Genomics

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The type II secretion system (T2SS) plays a major role in promoting bacterial survival in the environment and in human hosts. One of the best characterized T2SS is that of Legionella pneumophila , the agent of Legionnaires’ disease. Secreting at least 25 proteins, including degradative enzymes, eukaryotic-like proteins and novel effectors, this T2SS contributes to the ability of L. pneumophila to grow at low temperatures, infect amoebal and macrophage hosts, damage lung tissue, evade the immune system, and undergo sliding motility. The genes encoding the T2SS are conserved across the genus Legionella , which includes 62 species and >30 pathogens in addition to L. pneumophila . The vast majority of effectors associated with L. pneumophila are shared by a large number of Legionella species, hinting at a critical role for them in the ecology of Legionella as a whole. However, no other species has the same repertoire as L. pneumophila , with, as a general rule, phylogenetically more closely related species sharing similar sets of effectors. T2SS effectors that are involved in infection of a eukaryotic host(s) are more prevalent throughout Legionella , indicating that they are under stronger selective pressure. The Legionella T2SS apparatus is closest to that of Aquicella (another parasite of amoebae), and a significant number of L. pneumophila effectors have their closest homologues in Aquicella . Thus, the T2SS of L. pneumophila probably originated within the order Legionellales , with some of its effectors having arisen within that Aquicella -like progenitor, while other effectors derived from the amoebal host, mimiviruses, fungi and less closely related bacteria.

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The Importance of Revisiting Legionellales Diversity

Cited by 28 publications

References 77 publications

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

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

Two intracellular and cell type-specific bacterial symbionts in the placozoan Trichoplax H2

Assessing the impact, genomics and evolution of type II secretion across a large, medically important genus: the Legionella type II secretion paradigm

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