Lack of methylated hopanoids renders the cyanobacterium Nostoc punctiforme sensitive to osmotic and pH stress

Tamsyn J. Garby, Emily D. Matys, Sarah E. Ongley, Anya Salih, Anthony W.D. Larkum, Malcolm R. Walter, Roger E. Summons, Brett A. Neilan

Research output: Contribution to journalArticleResearchpeer-review

Abstract

To investigate the function of 2-methylhopanoids in modern cyanobacteria, the hpnP gene coding for the radical S-adenosyl methionine (SAM) methylase protein that acts on the C-2 position of hopanoids was deleted from the filamentous cyanobacterium Nostoc punctiforme ATCC 29133S. The resulting ΔhpnP mutant lacked all 2-methylhopanoids but was found to produce much higher levels of two bacteriohopanepentol isomers than the wild type. Growth rates of the ΔhpnP mutant cultures were not significantly different from those of the wild type under standard growth conditions. Akinete formation was also not impeded by the absence of 2-methylhopanoids. The relative abundances of the different hopanoid structures in akinete-dominated cultures of the wild-type and ΔhpnP mutant strains were similar to those of vegetative cell-dominated cultures. However, the ΔhpnP mutant was found to have decreased growth rates under both pH and osmotic stress, confirming a role for 2-methylhopanoids in stress tolerance. Evidence of elevated photosystem II yield and NAD(P)H-dependent oxidoreductase activity in the ΔhpnP mutant under stress conditions, compared to the wild type, suggested that the absence of 2-methylhopanoids increases cellular metabolic rates under stress conditions.


IMPORTANCE As the first group of organisms to develop oxygenic photosynthesis, Cyanobacteria are central to the evolutionary history of life on Earth and the subsequent oxygenation of the atmosphere. To investigate the origin of cyanobacteria and the emergence of oxygenic photosynthesis, geobiologists use biomarkers, the remnants of lipids produced by different organisms that are found in geologic sediments. 2-Methylhopanes have been considered indicative of cyanobacteria in some environmental settings, with the parent lipids 2-methylhopanoids being present in many contemporary cyanobacteria. We have created a Nostoc punctiforme ΔhpnP mutant strain that does not produce 2-methylhopanoids to assess the influence of 2-methylhopanoids on stress tolerance. Increased metabolic activity in the mutant under stress indicates compensatory alterations in metabolism in the absence of 2-methylhopanoids.

LanguageEnglish
Article numbere00777-17
Pages1-15
Number of pages15
JournalApplied and Environmental Microbiology
Volume83
Issue number13
DOIs
Publication statusPublished - Jul 2017
Externally publishedYes

Fingerprint

Nostoc punctiforme
Nostoc
hopanoid
Osmotic Pressure
Cyanobacteria
cyanobacterium
mutants
Photosynthesis
stress tolerance
Growth
Protein Methyltransferases
photosynthesis
Geologic Sediments
Lipids
tolerance
lipid
Photosystem II Protein Complex
Atmosphere
vegetative cells
oxygenation

Keywords

  • BHP
  • BHT
  • cyanobacteria
  • hopanoid
  • nostoc punctiforme

Cite this

Garby, Tamsyn J. ; Matys, Emily D. ; Ongley, Sarah E. ; Salih, Anya ; Larkum, Anthony W.D. ; Walter, Malcolm R. ; Summons, Roger E. ; Neilan, Brett A. / Lack of methylated hopanoids renders the cyanobacterium Nostoc punctiforme sensitive to osmotic and pH stress. In: Applied and Environmental Microbiology. 2017 ; Vol. 83, No. 13. pp. 1-15.
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abstract = "To investigate the function of 2-methylhopanoids in modern cyanobacteria, the hpnP gene coding for the radical S-adenosyl methionine (SAM) methylase protein that acts on the C-2 position of hopanoids was deleted from the filamentous cyanobacterium Nostoc punctiforme ATCC 29133S. The resulting ΔhpnP mutant lacked all 2-methylhopanoids but was found to produce much higher levels of two bacteriohopanepentol isomers than the wild type. Growth rates of the ΔhpnP mutant cultures were not significantly different from those of the wild type under standard growth conditions. Akinete formation was also not impeded by the absence of 2-methylhopanoids. The relative abundances of the different hopanoid structures in akinete-dominated cultures of the wild-type and ΔhpnP mutant strains were similar to those of vegetative cell-dominated cultures. However, the ΔhpnP mutant was found to have decreased growth rates under both pH and osmotic stress, confirming a role for 2-methylhopanoids in stress tolerance. Evidence of elevated photosystem II yield and NAD(P)H-dependent oxidoreductase activity in the ΔhpnP mutant under stress conditions, compared to the wild type, suggested that the absence of 2-methylhopanoids increases cellular metabolic rates under stress conditions.IMPORTANCE As the first group of organisms to develop oxygenic photosynthesis, Cyanobacteria are central to the evolutionary history of life on Earth and the subsequent oxygenation of the atmosphere. To investigate the origin of cyanobacteria and the emergence of oxygenic photosynthesis, geobiologists use biomarkers, the remnants of lipids produced by different organisms that are found in geologic sediments. 2-Methylhopanes have been considered indicative of cyanobacteria in some environmental settings, with the parent lipids 2-methylhopanoids being present in many contemporary cyanobacteria. We have created a Nostoc punctiforme ΔhpnP mutant strain that does not produce 2-methylhopanoids to assess the influence of 2-methylhopanoids on stress tolerance. Increased metabolic activity in the mutant under stress indicates compensatory alterations in metabolism in the absence of 2-methylhopanoids.",
keywords = "BHP, BHT, cyanobacteria, hopanoid, nostoc punctiforme",
author = "Garby, {Tamsyn J.} and Matys, {Emily D.} and Ongley, {Sarah E.} and Anya Salih and Larkum, {Anthony W.D.} and Walter, {Malcolm R.} and Summons, {Roger E.} and Neilan, {Brett A.}",
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Garby, TJ, Matys, ED, Ongley, SE, Salih, A, Larkum, AWD, Walter, MR, Summons, RE & Neilan, BA 2017, 'Lack of methylated hopanoids renders the cyanobacterium Nostoc punctiforme sensitive to osmotic and pH stress', Applied and Environmental Microbiology, vol. 83, no. 13, e00777-17, pp. 1-15. https://doi.org/10.1128/AEM.00777-17

Lack of methylated hopanoids renders the cyanobacterium Nostoc punctiforme sensitive to osmotic and pH stress. / Garby, Tamsyn J.; Matys, Emily D.; Ongley, Sarah E.; Salih, Anya; Larkum, Anthony W.D.; Walter, Malcolm R.; Summons, Roger E.; Neilan, Brett A.

In: Applied and Environmental Microbiology, Vol. 83, No. 13, e00777-17, 07.2017, p. 1-15.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Lack of methylated hopanoids renders the cyanobacterium Nostoc punctiforme sensitive to osmotic and pH stress

AU - Garby, Tamsyn J.

AU - Matys, Emily D.

AU - Ongley, Sarah E.

AU - Salih, Anya

AU - Larkum, Anthony W.D.

AU - Walter, Malcolm R.

AU - Summons, Roger E.

AU - Neilan, Brett A.

PY - 2017/7

Y1 - 2017/7

N2 - To investigate the function of 2-methylhopanoids in modern cyanobacteria, the hpnP gene coding for the radical S-adenosyl methionine (SAM) methylase protein that acts on the C-2 position of hopanoids was deleted from the filamentous cyanobacterium Nostoc punctiforme ATCC 29133S. The resulting ΔhpnP mutant lacked all 2-methylhopanoids but was found to produce much higher levels of two bacteriohopanepentol isomers than the wild type. Growth rates of the ΔhpnP mutant cultures were not significantly different from those of the wild type under standard growth conditions. Akinete formation was also not impeded by the absence of 2-methylhopanoids. The relative abundances of the different hopanoid structures in akinete-dominated cultures of the wild-type and ΔhpnP mutant strains were similar to those of vegetative cell-dominated cultures. However, the ΔhpnP mutant was found to have decreased growth rates under both pH and osmotic stress, confirming a role for 2-methylhopanoids in stress tolerance. Evidence of elevated photosystem II yield and NAD(P)H-dependent oxidoreductase activity in the ΔhpnP mutant under stress conditions, compared to the wild type, suggested that the absence of 2-methylhopanoids increases cellular metabolic rates under stress conditions.IMPORTANCE As the first group of organisms to develop oxygenic photosynthesis, Cyanobacteria are central to the evolutionary history of life on Earth and the subsequent oxygenation of the atmosphere. To investigate the origin of cyanobacteria and the emergence of oxygenic photosynthesis, geobiologists use biomarkers, the remnants of lipids produced by different organisms that are found in geologic sediments. 2-Methylhopanes have been considered indicative of cyanobacteria in some environmental settings, with the parent lipids 2-methylhopanoids being present in many contemporary cyanobacteria. We have created a Nostoc punctiforme ΔhpnP mutant strain that does not produce 2-methylhopanoids to assess the influence of 2-methylhopanoids on stress tolerance. Increased metabolic activity in the mutant under stress indicates compensatory alterations in metabolism in the absence of 2-methylhopanoids.

AB - To investigate the function of 2-methylhopanoids in modern cyanobacteria, the hpnP gene coding for the radical S-adenosyl methionine (SAM) methylase protein that acts on the C-2 position of hopanoids was deleted from the filamentous cyanobacterium Nostoc punctiforme ATCC 29133S. The resulting ΔhpnP mutant lacked all 2-methylhopanoids but was found to produce much higher levels of two bacteriohopanepentol isomers than the wild type. Growth rates of the ΔhpnP mutant cultures were not significantly different from those of the wild type under standard growth conditions. Akinete formation was also not impeded by the absence of 2-methylhopanoids. The relative abundances of the different hopanoid structures in akinete-dominated cultures of the wild-type and ΔhpnP mutant strains were similar to those of vegetative cell-dominated cultures. However, the ΔhpnP mutant was found to have decreased growth rates under both pH and osmotic stress, confirming a role for 2-methylhopanoids in stress tolerance. Evidence of elevated photosystem II yield and NAD(P)H-dependent oxidoreductase activity in the ΔhpnP mutant under stress conditions, compared to the wild type, suggested that the absence of 2-methylhopanoids increases cellular metabolic rates under stress conditions.IMPORTANCE As the first group of organisms to develop oxygenic photosynthesis, Cyanobacteria are central to the evolutionary history of life on Earth and the subsequent oxygenation of the atmosphere. To investigate the origin of cyanobacteria and the emergence of oxygenic photosynthesis, geobiologists use biomarkers, the remnants of lipids produced by different organisms that are found in geologic sediments. 2-Methylhopanes have been considered indicative of cyanobacteria in some environmental settings, with the parent lipids 2-methylhopanoids being present in many contemporary cyanobacteria. We have created a Nostoc punctiforme ΔhpnP mutant strain that does not produce 2-methylhopanoids to assess the influence of 2-methylhopanoids on stress tolerance. Increased metabolic activity in the mutant under stress indicates compensatory alterations in metabolism in the absence of 2-methylhopanoids.

KW - BHP

KW - BHT

KW - cyanobacteria

KW - hopanoid

KW - nostoc punctiforme

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DO - 10.1128/AEM.00777-17

M3 - Article

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JF - Applied and Environmental Microbiology

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