Anammox Planctomycetes have a peptidoglycan cell wall

Teeseling, Muriel C. F. van; Mesman, Rob; Kuru, Erkin; Espaillat, Akbar; Cava, Felipe; Brun, Yves V.; VanNieuwenhze, Michael S.; Kartal, Boran; Niftrik, Laura van

doi:10.1038/ncomms7878

Cited by 209 publications

(122 citation statements)

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“…Most recently, the detection of peptidoglycan in the cell wall of planctomycetes, including G. obscuriglobus (16,17), supports the interpretation of the G. obscuriglobus cell plan as Gram negative. The absence of peptidoglycan and presence of a proteinaceous cell wall (18) had long been distinguishing planctomycete features that led to the proposal of a unique cell plan for all planctomycetes (3,5,6,13,19).…”

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confidence: 86%

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Global and Targeted Lipid Analysis of Gemmata obscuriglobus Reveals the Presence of Lipopolysaccharide, a Signature of the Classical Gram-Negative Outer Membrane

et al. 2016

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Planctomycete bacteria possess many unusual cellular properties, contributing to a cell plan long considered to be unique among the bacteria. However, data from recent studies are more consistent with a modified Gram-negative cell plan. A key feature of the Gram-negative plan is the presence of an outer membrane (OM), for which lipopolysaccharide (LPS) is a signature molecule. Despite genomic evidence for an OM in planctomycetes, no biochemical verification has been reported. We attempted to detect and characterize LPS in the planctomycete Gemmata obscuriglobus. We obtained direct evidence for LPS and lipid A using electrophoresis and differential staining. Gas chromatography-mass spectrometry (GC-MS) compositional analysis of LPS extracts identified eight different 3-hydroxy fatty acids (3-HOFAs), 2-keto 3-deoxy-D-manno-octulosonic acid (Kdo), glucosamine, and hexose and heptose sugars, a chemical profile unique to Gram-negative LPS. Combined with molecular/structural information collected from matrix-assisted laser desorption ionization-time of flight (MALDI-TOF) MS analysis of putative intact lipid A, these data led us to propose a heterogeneous hexa-acylated lipid A structure (multiple-lipid A species). We also confirmed previous reports of G. obscuriglobus whole-cell fatty acid (FA) and sterol compositions and detected a novel polyunsaturated FA (PUFA). Our confirmation of LPS, and by implication an OM, in G. obscuriglobus raises the possibility that other planctomycetes possess an OM. The pursuit of this question, together with studies of the structural connections between planctomycete LPS and peptidoglycans, will shed more light on what appears to be a planctomycete variation on the Gram-negative cell plan. IMPORTANCEBacterial species are classified as Gram positive or negative based on their cell envelope structure. For 25 years, the envelope of planctomycete bacteria has been considered a unique exception, as it lacks peptidoglycan and an outer membrane (OM). However, the very recent detection of peptidoglycan in planctomycete species has provided evidence for a more conventional cell wall and raised questions about other elements of the cell envelope. Here, we report direct evidence of lipopolysaccharide in the planctomycete G. obscuriglobus, suggesting the presence of an OM and supporting the proposal that the planctomycete cell envelope is an extension of the canonical Gram-negative plan. This interpretation features a convoluted cytoplasmic membrane and expanded periplasmic space, the functions of which provide an intriguing avenue for future investigation.T he planctomycete bacterium Gemmata obscuriglobus (1) is of considerable interest to the fields of cell and evolutionary biology due to its uncommon cellular features and evolutionary placement within the Bacteria (2-5). G. obscuriglobus possesses an extensive endomembrane system (6) with superficial eukaryotelike properties, including the presence of membrane coat-like (MC-like) proteins (7), large quantities of sterols (8, 9), a propos...

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confidence: 86%

“…The pursuit of this question, together with studies of the structural connections between the LPS of G. obscuriglobus (and possibly other planctomycetes) and the newly discovered planctomycete peptidoglycans (16,17), will shed more light on what is now emerging as the planctomycete variation on the Gram-negative cell plan (20). …”

Section: Discussionmentioning

confidence: 99%

Global and Targeted Lipid Analysis of Gemmata obscuriglobus Reveals the Presence of Lipopolysaccharide, a Signature of the Classical Gram-Negative Outer Membrane

et al. 2016

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“…Various publications have recently revealed the presence of PG in some planctomycetal and chlamydial species, suggesting that it is also present in other species in these phyla and in other PVC phyla (Pilhofer et al, 2013; Liechti et al, 2014, 2016; Jeske et al, 2015; van Teeseling et al, 2015). Furthermore, a link between PG synthesis at the septum and division in Chlamydiae is emerging, offering clues about the mechanism of bacterial division without FtsZ (Liechti et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Evolutionary Cell Biology of Division Mode in the Bacterial Planctomycetes-Verrucomicrobia- Chlamydiae Superphylum

2016

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Bacteria from the Planctomycetes, Verrucomicrobia, and Chlamydiae (PVC) superphylum are exceptions to the otherwise dominant mode of division by binary fission, which is based on the interaction between the FtsZ protein and the peptidoglycan (PG) biosynthesis machinery. Some PVC bacteria are deprived of the FtsZ protein and were also thought to lack PG. How these bacteria divide is still one of the major mysteries of microbiology. The presence of PG has recently been revealed in Planctomycetes and Chlamydiae, and proteins related to PG synthesis have been shown to be implicated in the division process in Chlamydiae, providing important insights into PVC mechanisms of division. Here, we review the historical lack of observation of PG in PVC bacteria, its recent detection in two phyla and its involvement in chlamydial cell division. Based on the detection of PG-related proteins in PVC proteomes, we consider the possible evolution of the diverse division mechanisms in these bacteria. We conclude by summarizing what is known and what remains to be understood about the evolutionary cell biology of PVC division modes.

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“…Similar to Chlamydia, the anammox bacteria were proposed to lack peptidoglycan because no peptidoglycan layer was observed in resin-embedded sections of either high-pressure frozen and freeze-substituted or chemically fixed anammox cells (Lindsay et al, 2001). However, cryo-transmission electron microscopy and metabolic labeling with EDA-DA revealed a peptidoglycan layer in anammox bacteria (van Teeseling et al, 2015). Therefore, cryotransmission electron microscopy may also be capable of detecting plastid peptidoglycan in moss.…”

Section: Peptidoglycan-surrounded Plastidsmentioning

confidence: 99%

Moss Chloroplasts Are Surrounded by a Peptidoglycan Wall Containing D-Amino Acids

et al. 2016

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It is believed that the plastids in green plants lost peptidoglycan (i.e., a bacterial cell wall-containing D-amino acids) during their evolution from an endosymbiotic cyanobacterium. Although wall-like structures could not be detected in the plastids of green plants, the moss Physcomitrella patens has the genes required to generate peptidoglycan (Mur genes), and knocking out these genes causes defects in chloroplast division. Here, we generated P. patens knockout lines (ΔPp-ddl) for a homolog of the bacterial peptidoglycan-synthetic gene encoding D-Ala:D-Ala ligase. ΔPp-ddl had a macrochloroplast phenotype, similar to other Mur knockout lines. The addition of D-Ala-D-Ala (DA-DA) to the medium suppressed the appearance of giant chloroplasts in ΔPp-ddl, but the addition of L-Ala-L-Ala (LA-LA), DA-LA, LA-DA, or D-Ala did not. Recently, a metabolic method for labeling bacterial peptidoglycan was established using ethynyl-DA-DA (EDA-DA) and click chemistry to attach an azidemodified fluorophore to the ethynyl group. The ΔPp-ddl line complemented with EDA-DA showed that moss chloroplasts are completely surrounded by peptidoglycan. Our findings strongly suggest that the moss plastids have a peptidoglycan wall containing D-amino acids. By contrast, no plastid phenotypes were observed in the T-DNA tagged ddl mutant lines of Arabidopsis thaliana.

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Anammox Planctomycetes have a peptidoglycan cell wall

Cited by 209 publications

References 43 publications

Global and Targeted Lipid Analysis of Gemmata obscuriglobus Reveals the Presence of Lipopolysaccharide, a Signature of the Classical Gram-Negative Outer Membrane

Global and Targeted Lipid Analysis of Gemmata obscuriglobus Reveals the Presence of Lipopolysaccharide, a Signature of the Classical Gram-Negative Outer Membrane

Evolutionary Cell Biology of Division Mode in the Bacterial Planctomycetes-Verrucomicrobia- Chlamydiae Superphylum

Moss Chloroplasts Are Surrounded by a Peptidoglycan Wall Containing D-Amino Acids

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