An Evolutionary Arms Race Between Burkholderia pseudomallei and Host Immune System: What Do We Know?

Chomkatekaew, Chalita; Boonklang, Phumrapee; Sangphukieo, Apiwat; Chewapreecha, Claire

doi:10.3389/fmicb.2020.612568

Cited by 8 publications

(5 citation statements)

References 196 publications

(230 reference statements)

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“…Family 1 peroxidase operons are widely distributed in Mycobacteria, including M. tuberculosis and M. leprae, the causative agents of tuberculosis and leprosy, respectively 90,91 . Flp and desulfurase systems are both found in Burkholderia cepacia (pulmonary infections, cystic fibrosis) and Burkholderia pseudomallei (melioidosis) 92 while Nocardia spp. (nocardiosis), Bordetella spp.…”

Section: Resultsmentioning

confidence: 99%

Large-scale computational discovery and analysis of virus-derived microbial nanocompartments

Andreas

Giessen

2021

Nat Commun

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Encapsulins are a class of microbial protein compartments defined by the viral HK97-fold of their capsid protein, self-assembly into icosahedral shells, and dedicated cargo loading mechanism for sequestering specific enzymes. Encapsulins are often misannotated and traditional sequence-based searches yield many false positive hits in the form of phage capsids. Here, we develop an integrated search strategy to carry out a large-scale computational analysis of prokaryotic genomes with the goal of discovering an exhaustive and curated set of all HK97-fold encapsulin-like systems. We find over 6,000 encapsulin-like systems in 31 bacterial and four archaeal phyla, including two novel encapsulin families. We formulate hypotheses about their potential biological functions and biomedical relevance, which range from natural product biosynthesis and stress resistance to carbon metabolism and anaerobic hydrogen production. An evolutionary analysis of encapsulins and related HK97-type virus families shows that they share a common ancestor, and we conclude that encapsulins likely evolved from HK97-type bacteriophages.

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Section: Resultsmentioning

confidence: 99%

Large-scale computational discovery and analysis of virus-derived microbial nanocompartments

Andreas

Giessen

2021

Nat Commun

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“…Many Family 1 Flp and Family 2 desulfurase systems are found in Burkholderia species, including the pathogens Burkholderia cepacia (pulmonary infections and cystic fibrosis) and Burkholderia pseudomallei (melioidosis) (136), while Nocardia spp. (nocardiosis), Clostridium spp.…”

Section: Biomedical and Agricultural Relevancementioning

confidence: 99%

Encapsulins

Giessen

2022

Annu. Rev. Biochem.

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Subcellular compartmentalization is a defining feature of all cells. In prokaryotes, compartmentalization is generally achieved via protein-based strategies. The two main classes of microbial protein compartments are bacterial microcompartments and encapsulin nanocompartments. Encapsulins self-assemble into proteinaceous shells with diameters between 24 and 42 nm and are defined by the viral HK97-fold of their shell protein. Encapsulins have the ability to encapsulate dedicated cargo proteins, including ferritin-like proteins, peroxidases, and desulfurases. Encapsulation is mediated by targeting sequences present in all cargo proteins. Encapsulins are found in many bacterial and archaeal phyla and have been suggested to play roles in iron storage, stress resistance, sulfur metabolism, and natural product biosynthesis. Phylogenetic analyses indicate that they share a common ancestor with viral capsid proteins. Many pathogens encode encapsulins, and recent evidence suggests that they may contribute toward pathogenicity. The existing information on encapsulin structure, biochemistry, biological function, and biomedical relevance is reviewed here. Expected final online publication date for the Annual Review of Biochemistry, Volume 91 is June 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

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“…It is possible that different BPSL1661 alleles may facilitate bacterial adherence to different surfaces, cells, or hosts. This attachment could lead to biofilm formation or the bacterium being internalized by host cells, both of which are known bacterial strategies to withstand nutrient deprivation ( Brown et al 2008 ; Petrova and Sauer 2012 ; Chomkatekaew et al 2020 ). Our study has a strong implication that the presence of B. pseudomallei in nutrient-depleted soil may define geographical regions where humans are at risk of melioidosis.…”

Section: Discussionmentioning

confidence: 99%

Co-evolutionary Signals IdentifyBurkholderia pseudomalleiSurvival Strategies in a Hostile Environment

Chewapreecha

Pensar

Chattagul

et al. 2021

Molecular Biology and Evolution

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The soil bacterium Burkholderia pseudomallei is the causative agent of melioidosis and a significant cause of human morbidity and mortality in many tropical and subtropical countries. The species notoriously survives harsh environmental conditions but the genetic architecture for these adaptations remains unclear. Here we employed a powerful combination of genome-wide epistasis and co-selection studies (2,011 genomes), condition-wide transcriptome analyses (82 diverse conditions), and a gene knockout assay to uncover signals of “co-selection”—that is a combination of genetic markers that have been repeatedly selected together through B. pseudomallei evolution. These enabled us to identify 13,061 mutation pairs under co-selection in distinct genes and noncoding RNA. Genes under co-selection displayed marked expression correlation when B. pseudomallei was subjected to physical stress conditions, highlighting the conditions as one of the major evolutionary driving forces for this bacterium. We identified a putative adhesin (BPSL1661) as a hub of co-selection signals, experimentally confirmed a BPSL1661 role under nutrient deprivation, and explored the functional basis of co-selection gene network surrounding BPSL1661 in facilitating the bacterial survival under nutrient depletion. Our findings suggest that nutrient-limited conditions have been the common selection pressure acting on this species, and allelic variation of BPSL1661 may have promoted B. pseudomallei survival during harsh environmental conditions by facilitating bacterial adherence to different surfaces, cells, or living hosts.

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An Evolutionary Arms Race Between Burkholderia pseudomallei and Host Immune System: What Do We Know?

Cited by 8 publications

References 196 publications

Large-scale computational discovery and analysis of virus-derived microbial nanocompartments

Large-scale computational discovery and analysis of virus-derived microbial nanocompartments

Encapsulins

Co-evolutionary Signals IdentifyBurkholderia pseudomalleiSurvival Strategies in a Hostile Environment

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