Contrasting strategies used by lichen microalgae to cope with desiccation-rehydration stress revealed by metabolite profiling and cell wall analysis

Summary Most lichens in general, and their phycobionts in particular, are desiccation tolerant, but their mechanisms of desiccation tolerance (DT) remain obscure. The physiological responses and cell wall features of two putatively contrasting lichen‐forming microalgae, Trebouxia sp. TR9 (TR9), isol...

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Published inEnvironmental microbiology Vol. 18; no. 5; pp. 1546 - 1560
Main Authors Centeno, Danilo C., Hell, Aline F., Braga, Marcia R., del Campo, Eva M., Casano, Leonardo M.
Format Journal Article
LanguageEnglish
Published England Blackwell Publishing Ltd 01.05.2016
Wiley Subscription Services, Inc
Subjects
Algae
Ascomycota - physiology
ascorbic acid
Cell Wall - physiology
cell walls
Chlorophyta - physiology
Coccomyxa
Dehydration
Desiccation
drought tolerance
Gene Expression Regulation, Plant - physiology
habitats
Lichens
Lichens - classification
Limestone
Metabolites
Microalgae
Microalgae - physiology
oligosaccharides
phenolic compounds
Phenols
physiological response
Physiological responses
polyols
Ramalina
Ramalina farinacea
Solorina
Stress, Physiological
Symbiosis
Trebouxia
Water - metabolism
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Abstract Summary Most lichens in general, and their phycobionts in particular, are desiccation tolerant, but their mechanisms of desiccation tolerance (DT) remain obscure. The physiological responses and cell wall features of two putatively contrasting lichen‐forming microalgae, Trebouxia sp. TR9 (TR9), isolated from Ramalina farinacea (adapted to frequent desiccation‐rehydration cycles), and Coccomyxa solorina‐saccatae (Csol), obtained from Solorina saccata (growing in usually humid limestone crevices, subjected to seasonal dry periods) was characterized. Microalgal cultures were desiccated under 25%–30% RH and then rehydrated. Under these conditions, RWC and ψw decreased faster and simultaneously during dehydration in Csol, whereas TR9 maintained its ψw until 70% RWC. The metabolic profile indicated that polyols played a key role in DT of both microalgae. However, TR9 constitutively accumulated higher amounts of polyols, whereas Csol induced the polyol synthesis under desiccation–rehydration. Csol also accumulated ascorbic acid, while TR9 synthesized protective raffinose‐family oligosaccharides (RFOs) and increased its content of phenolics. Additionally, TR9 exhibited thicker and qualitatively different cell wall and extracellular polymeric layer compared with Csol, indicating higher water retention capability. The findings were consistent with the notion that lichen microalgae would have evolved distinct strategies to cope with desiccation–rehydration stress in correspondence with the water regime of their respective habitats.
AbstractList Most lichens in general, and their phycobionts in particular, are desiccation tolerant, but their mechanisms of desiccation tolerance (DT) remain obscure. The physiological responses and cell wall features of two putatively contrasting lichen-forming microalgae, Trebouxia sp. TR9 (TR9), isolated from Ramalina farinacea (adapted to frequent desiccation-rehydration cycles), and Coccomyxa solorina-saccatae (Csol), obtained from Solorina saccata (growing in usually humid limestone crevices, subjected to seasonal dry periods) was characterized. Microalgal cultures were desiccated under 25%-30% RH and then rehydrated. Under these conditions, RWC and ψw decreased faster and simultaneously during dehydration in Csol, whereas TR9 maintained its ψw until 70% RWC. The metabolic profile indicated that polyols played a key role in DT of both microalgae. However, TR9 constitutively accumulated higher amounts of polyols, whereas Csol induced the polyol synthesis under desiccation-rehydration. Csol also accumulated ascorbic acid, while TR9 synthesized protective raffinose-family oligosaccharides (RFOs) and increased its content of phenolics. Additionally, TR9 exhibited thicker and qualitatively different cell wall and extracellular polymeric layer compared with Csol, indicating higher water retention capability. The findings were consistent with the notion that lichen microalgae would have evolved distinct strategies to cope with desiccation-rehydration stress in correspondence with the water regime of their respective habitats.Most lichens in general, and their phycobionts in particular, are desiccation tolerant, but their mechanisms of desiccation tolerance (DT) remain obscure. The physiological responses and cell wall features of two putatively contrasting lichen-forming microalgae, Trebouxia sp. TR9 (TR9), isolated from Ramalina farinacea (adapted to frequent desiccation-rehydration cycles), and Coccomyxa solorina-saccatae (Csol), obtained from Solorina saccata (growing in usually humid limestone crevices, subjected to seasonal dry periods) was characterized. Microalgal cultures were desiccated under 25%-30% RH and then rehydrated. Under these conditions, RWC and ψw decreased faster and simultaneously during dehydration in Csol, whereas TR9 maintained its ψw until 70% RWC. The metabolic profile indicated that polyols played a key role in DT of both microalgae. However, TR9 constitutively accumulated higher amounts of polyols, whereas Csol induced the polyol synthesis under desiccation-rehydration. Csol also accumulated ascorbic acid, while TR9 synthesized protective raffinose-family oligosaccharides (RFOs) and increased its content of phenolics. Additionally, TR9 exhibited thicker and qualitatively different cell wall and extracellular polymeric layer compared with Csol, indicating higher water retention capability. The findings were consistent with the notion that lichen microalgae would have evolved distinct strategies to cope with desiccation-rehydration stress in correspondence with the water regime of their respective habitats.
Most lichens in general, and their phycobionts in particular, are desiccation tolerant, but their mechanisms of desiccation tolerance (DT) remain obscure. The physiological responses and cell wall features of two putatively contrasting lichen‐forming microalgae, Trebouxia sp. TR9 (TR9), isolated from Ramalina farinacea (adapted to frequent desiccation‐rehydration cycles), and Coccomyxa solorina‐saccatae ( Csol ), obtained from Solorina saccata (growing in usually humid limestone crevices, subjected to seasonal dry periods) was characterized. Microalgal cultures were desiccated under 25%–30% RH and then rehydrated. Under these conditions, RWC and ψ w decreased faster and simultaneously during dehydration in Cso l, whereas TR9 maintained its ψ w until 70% RWC. The metabolic profile indicated that polyols played a key role in DT of both microalgae. However, TR9 constitutively accumulated higher amounts of polyols, whereas Csol induced the polyol synthesis under desiccation–rehydration. Csol also accumulated ascorbic acid, while TR9 synthesized protective raffinose‐family oligosaccharides (RFOs) and increased its content of phenolics. Additionally, TR9 exhibited thicker and qualitatively different cell wall and extracellular polymeric layer compared with Csol , indicating higher water retention capability. The findings were consistent with the notion that lichen microalgae would have evolved distinct strategies to cope with desiccation–rehydration stress in correspondence with the water regime of their respective habitats.
Most lichens in general, and their phycobionts in particular, are desiccation tolerant, but their mechanisms of desiccation tolerance (DT) remain obscure. The physiological responses and cell wall features of two putatively contrasting lichen-forming microalgae, Trebouxia sp. TR9 (TR9), isolated from Ramalina farinacea (adapted to frequent desiccation-rehydration cycles), and Coccomyxa solorina-saccatae (Csol), obtained from Solorina saccata (growing in usually humid limestone crevices, subjected to seasonal dry periods) was characterized. Microalgal cultures were desiccated under 25%-30% RH and then rehydrated. Under these conditions, RWC and ψw decreased faster and simultaneously during dehydration in Csol, whereas TR9 maintained its ψw until 70% RWC. The metabolic profile indicated that polyols played a key role in DT of both microalgae. However, TR9 constitutively accumulated higher amounts of polyols, whereas Csol induced the polyol synthesis under desiccation-rehydration. Csol also accumulated ascorbic acid, while TR9 synthesized protective raffinose-family oligosaccharides (RFOs) and increased its content of phenolics. Additionally, TR9 exhibited thicker and qualitatively different cell wall and extracellular polymeric layer compared with Csol, indicating higher water retention capability. The findings were consistent with the notion that lichen microalgae would have evolved distinct strategies to cope with desiccation-rehydration stress in correspondence with the water regime of their respective habitats.
Summary Most lichens in general, and their phycobionts in particular, are desiccation tolerant, but their mechanisms of desiccation tolerance (DT) remain obscure. The physiological responses and cell wall features of two putatively contrasting lichen-forming microalgae, Trebouxia sp. TR9 (TR9), isolated from Ramalina farinacea (adapted to frequent desiccation-rehydration cycles), and Coccomyxa solorina-saccatae (Csol), obtained from Solorina saccata (growing in usually humid limestone crevices, subjected to seasonal dry periods) was characterized. Microalgal cultures were desiccated under 25%-30% RH and then rehydrated. Under these conditions, RWC and ψw decreased faster and simultaneously during dehydration in Csol, whereas TR9 maintained its ψw until 70% RWC. The metabolic profile indicated that polyols played a key role in DT of both microalgae. However, TR9 constitutively accumulated higher amounts of polyols, whereas Csol induced the polyol synthesis under desiccation-rehydration. Csol also accumulated ascorbic acid, while TR9 synthesized protective raffinose-family oligosaccharides (RFOs) and increased its content of phenolics. Additionally, TR9 exhibited thicker and qualitatively different cell wall and extracellular polymeric layer compared with Csol, indicating higher water retention capability. The findings were consistent with the notion that lichen microalgae would have evolved distinct strategies to cope with desiccation-rehydration stress in correspondence with the water regime of their respective habitats.
Summary Most lichens in general, and their phycobionts in particular, are desiccation tolerant, but their mechanisms of desiccation tolerance (DT) remain obscure. The physiological responses and cell wall features of two putatively contrasting lichen‐forming microalgae, Trebouxia sp. TR9 (TR9), isolated from Ramalina farinacea (adapted to frequent desiccation‐rehydration cycles), and Coccomyxa solorina‐saccatae (Csol), obtained from Solorina saccata (growing in usually humid limestone crevices, subjected to seasonal dry periods) was characterized. Microalgal cultures were desiccated under 25%–30% RH and then rehydrated. Under these conditions, RWC and ψw decreased faster and simultaneously during dehydration in Csol, whereas TR9 maintained its ψw until 70% RWC. The metabolic profile indicated that polyols played a key role in DT of both microalgae. However, TR9 constitutively accumulated higher amounts of polyols, whereas Csol induced the polyol synthesis under desiccation–rehydration. Csol also accumulated ascorbic acid, while TR9 synthesized protective raffinose‐family oligosaccharides (RFOs) and increased its content of phenolics. Additionally, TR9 exhibited thicker and qualitatively different cell wall and extracellular polymeric layer compared with Csol, indicating higher water retention capability. The findings were consistent with the notion that lichen microalgae would have evolved distinct strategies to cope with desiccation–rehydration stress in correspondence with the water regime of their respective habitats.
Most lichens in general, and their phycobionts in particular, are desiccation tolerant, but their mechanisms of desiccation tolerance (DT) remain obscure. The physiological responses and cell wall features of two putatively contrasting lichen-forming microalgae, Trebouxia sp. TR9 (TR9), isolated from Ramalina farinacea (adapted to frequent desiccation-rehydration cycles), and Coccomyxa solorina-saccatae (Csol), obtained from Solorina saccata (growing in usually humid limestone crevices, subjected to seasonal dry periods) was characterized. Microalgal cultures were desiccated under 25%-30% RH and then rehydrated. Under these conditions, RWC and psi sub(w) decreased faster and simultaneously during dehydration in Csol, whereas TR9 maintained its psi sub(w) until 70% RWC. The metabolic profile indicated that polyols played a key role in DT of both microalgae. However, TR9 constitutively accumulated higher amounts of polyols, whereas Csol induced the polyol synthesis under desiccation-rehydration. Csol also accumulated ascorbic acid, while TR9 synthesized protective raffinose-family oligosaccharides (RFOs) and increased its content of phenolics. Additionally, TR9 exhibited thicker and qualitatively different cell wall and extracellular polymeric layer compared with Csol, indicating higher water retention capability. The findings were consistent with the notion that lichen microalgae would have evolved distinct strategies to cope with desiccation-rehydration stress in correspondence with the water regime of their respective habitats.
Author del Campo, Eva M.
Centeno, Danilo C.
Hell, Aline F.
Braga, Marcia R.
Casano, Leonardo M.
Author_xml – sequence: 1
  givenname: Danilo C.
  surname: Centeno
  fullname: Centeno, Danilo C.
  organization: Centre of Natural Sciences and Humanities, Federal University of ABC, 09606-070, São Bernardo do Campo, SP, Brazil
– sequence: 2
  givenname: Aline F.
  surname: Hell
  fullname: Hell, Aline F.
  organization: Department of Plant Physiology and Biochemistry, Institute of Botany, SP, 04301-912, São Paulo, Brazil
– sequence: 3
  givenname: Marcia R.
  surname: Braga
  fullname: Braga, Marcia R.
  organization: Department of Plant Physiology and Biochemistry, Institute of Botany, SP, 04301-912, São Paulo, Brazil
– sequence: 4
  givenname: Eva M.
  surname: del Campo
  fullname: del Campo, Eva M.
  organization: Department of Life Sciences, University of Alcalá, Alcalá de Henares (Madrid), 28805-, Spain
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  givenname: Leonardo M.
  surname: Casano
  fullname: Casano, Leonardo M.
  email: leonardo.casano@uah.es
  organization: Department of Life Sciences, University of Alcalá, Alcalá de Henares (Madrid), 28805-, Spain
BackLink https://www.ncbi.nlm.nih.gov/pubmed/26914009$$D View this record in MEDLINE/PubMed
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2009; 57
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2008; 231
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2009; 23
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2013; 41
2008
2010; 243
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1986; 18
2015; 208
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2007; 99
2007; 58
1999; 9
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2004; 312
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1999; 37
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2015
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Snippet Summary Most lichens in general, and their phycobionts in particular, are desiccation tolerant, but their mechanisms of desiccation tolerance (DT) remain...
Most lichens in general, and their phycobionts in particular, are desiccation tolerant, but their mechanisms of desiccation tolerance (DT) remain obscure. The...
Summary Most lichens in general, and their phycobionts in particular, are desiccation tolerant, but their mechanisms of desiccation tolerance (DT) remain...
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StartPage 1546
SubjectTerms Algae
Ascomycota - physiology
ascorbic acid
Cell Wall - physiology
cell walls
Chlorophyta - physiology
Coccomyxa
Dehydration
Desiccation
drought tolerance
Gene Expression Regulation, Plant - physiology
habitats
Lichens
Lichens - classification
Limestone
Metabolites
Microalgae
Microalgae - physiology
oligosaccharides
phenolic compounds
Phenols
physiological response
Physiological responses
polyols
Ramalina
Ramalina farinacea
Solorina
Stress, Physiological
Symbiosis
Trebouxia
Water - metabolism
Title Contrasting strategies used by lichen microalgae to cope with desiccation-rehydration stress revealed by metabolite profiling and cell wall analysis
URI https://api.istex.fr/ark:/67375/WNG-JX82WVS5-W/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1111%2F1462-2920.13249
https://www.ncbi.nlm.nih.gov/pubmed/26914009
https://www.proquest.com/docview/1784593729
https://www.proquest.com/docview/1785731971
https://www.proquest.com/docview/1794497435
https://www.proquest.com/docview/1825412680
Volume 18
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