Growth study under combined effects of temperature, pH and salinity and transcriptome analysis revealed adaptations of Aspergillus terreus NTOU4989 to the extreme conditions at Kueishan Island Hydrothermal Vent Field, Taiwan.

A high diversity of fungi was discovered on various substrates collected at the marine shallow-water Kueishan Island Hydrothermal Vent Field, Taiwan, using culture and metabarcoding methods but whether these fungi can grow and play an active role in such an extreme environment is unknown. We investi...

Full description

Bibliographic Details
Main Authors: Ka-Lai Pang, Michael Wai-Lun Chiang, Sheng-Yu Guo, Chi-Yu Shih, Hans U Dahms, Jiang-Shiou Hwang, Hyo-Jung Cha
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0233621
id doaj-ea5f8a7636be41be92cbf5758d3558dc
record_format Article
spelling doaj-ea5f8a7636be41be92cbf5758d3558dc2021-03-03T21:49:00ZengPublic Library of Science (PLoS)PLoS ONE1932-62032020-01-01155e023362110.1371/journal.pone.0233621Growth study under combined effects of temperature, pH and salinity and transcriptome analysis revealed adaptations of Aspergillus terreus NTOU4989 to the extreme conditions at Kueishan Island Hydrothermal Vent Field, Taiwan.Ka-Lai PangMichael Wai-Lun ChiangSheng-Yu GuoChi-Yu ShihHans U DahmsJiang-Shiou HwangHyo-Jung ChaA high diversity of fungi was discovered on various substrates collected at the marine shallow-water Kueishan Island Hydrothermal Vent Field, Taiwan, using culture and metabarcoding methods but whether these fungi can grow and play an active role in such an extreme environment is unknown. We investigated the combined effects of different salinity, temperature and pH on growth of ten fungi (in the genera Aspergillus, Penicillium, Fodinomyces, Microascus, Trichoderma, Verticillium) isolated from the sediment and the vent crab Xenograpsus testudinatus. The growth responses of the tested fungi could be referred to three groups: (1) wide pH, salinity and temperature ranges, (2) salinity-dependent and temperature-sensitive, and (3) temperature-tolerant. Aspergillus terreus NTOU4989 was the only fungus which showed growth at 45 °C, pH 3 and 30 ‰ salinity, and might be active near the vents. We also carried out a transcriptome analysis to understand the molecular adaptations of A. terreus NTOU4989 under these extreme conditions. Data revealed that stress-related genes were differentially expressed at high temperature (45 °C); for instance, mannitol biosynthetic genes were up-regulated while glutathione S-transferase and amino acid oxidase genes down-regulated in response to high temperature. On the other hand, hydrogen ion transmembrane transport genes and phenylalanine ammonia lyase were up-regulated while pH-response transcription factor was down-regulated at pH 3, a relative acidic environment. However, genes related to salt tolerance, such as glycerol lipid metabolism and mitogen-activated protein kinase, were up-regulated in both conditions, possibly related to maintaining water homeostasis. The results of this study revealed the genetic evidence of adaptation in A. terreus NTOU4989 to changes of environmental conditions.https://doi.org/10.1371/journal.pone.0233621
collection DOAJ
language English
format Article
sources DOAJ
author Ka-Lai Pang
Michael Wai-Lun Chiang
Sheng-Yu Guo
Chi-Yu Shih
Hans U Dahms
Jiang-Shiou Hwang
Hyo-Jung Cha
spellingShingle Ka-Lai Pang
Michael Wai-Lun Chiang
Sheng-Yu Guo
Chi-Yu Shih
Hans U Dahms
Jiang-Shiou Hwang
Hyo-Jung Cha
Growth study under combined effects of temperature, pH and salinity and transcriptome analysis revealed adaptations of Aspergillus terreus NTOU4989 to the extreme conditions at Kueishan Island Hydrothermal Vent Field, Taiwan.
PLoS ONE
author_facet Ka-Lai Pang
Michael Wai-Lun Chiang
Sheng-Yu Guo
Chi-Yu Shih
Hans U Dahms
Jiang-Shiou Hwang
Hyo-Jung Cha
author_sort Ka-Lai Pang
title Growth study under combined effects of temperature, pH and salinity and transcriptome analysis revealed adaptations of Aspergillus terreus NTOU4989 to the extreme conditions at Kueishan Island Hydrothermal Vent Field, Taiwan.
title_short Growth study under combined effects of temperature, pH and salinity and transcriptome analysis revealed adaptations of Aspergillus terreus NTOU4989 to the extreme conditions at Kueishan Island Hydrothermal Vent Field, Taiwan.
title_full Growth study under combined effects of temperature, pH and salinity and transcriptome analysis revealed adaptations of Aspergillus terreus NTOU4989 to the extreme conditions at Kueishan Island Hydrothermal Vent Field, Taiwan.
title_fullStr Growth study under combined effects of temperature, pH and salinity and transcriptome analysis revealed adaptations of Aspergillus terreus NTOU4989 to the extreme conditions at Kueishan Island Hydrothermal Vent Field, Taiwan.
title_full_unstemmed Growth study under combined effects of temperature, pH and salinity and transcriptome analysis revealed adaptations of Aspergillus terreus NTOU4989 to the extreme conditions at Kueishan Island Hydrothermal Vent Field, Taiwan.
title_sort growth study under combined effects of temperature, ph and salinity and transcriptome analysis revealed adaptations of aspergillus terreus ntou4989 to the extreme conditions at kueishan island hydrothermal vent field, taiwan.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2020-01-01
description A high diversity of fungi was discovered on various substrates collected at the marine shallow-water Kueishan Island Hydrothermal Vent Field, Taiwan, using culture and metabarcoding methods but whether these fungi can grow and play an active role in such an extreme environment is unknown. We investigated the combined effects of different salinity, temperature and pH on growth of ten fungi (in the genera Aspergillus, Penicillium, Fodinomyces, Microascus, Trichoderma, Verticillium) isolated from the sediment and the vent crab Xenograpsus testudinatus. The growth responses of the tested fungi could be referred to three groups: (1) wide pH, salinity and temperature ranges, (2) salinity-dependent and temperature-sensitive, and (3) temperature-tolerant. Aspergillus terreus NTOU4989 was the only fungus which showed growth at 45 °C, pH 3 and 30 ‰ salinity, and might be active near the vents. We also carried out a transcriptome analysis to understand the molecular adaptations of A. terreus NTOU4989 under these extreme conditions. Data revealed that stress-related genes were differentially expressed at high temperature (45 °C); for instance, mannitol biosynthetic genes were up-regulated while glutathione S-transferase and amino acid oxidase genes down-regulated in response to high temperature. On the other hand, hydrogen ion transmembrane transport genes and phenylalanine ammonia lyase were up-regulated while pH-response transcription factor was down-regulated at pH 3, a relative acidic environment. However, genes related to salt tolerance, such as glycerol lipid metabolism and mitogen-activated protein kinase, were up-regulated in both conditions, possibly related to maintaining water homeostasis. The results of this study revealed the genetic evidence of adaptation in A. terreus NTOU4989 to changes of environmental conditions.
url https://doi.org/10.1371/journal.pone.0233621
work_keys_str_mv AT kalaipang growthstudyundercombinedeffectsoftemperaturephandsalinityandtranscriptomeanalysisrevealedadaptationsofaspergillusterreusntou4989totheextremeconditionsatkueishanislandhydrothermalventfieldtaiwan
AT michaelwailunchiang growthstudyundercombinedeffectsoftemperaturephandsalinityandtranscriptomeanalysisrevealedadaptationsofaspergillusterreusntou4989totheextremeconditionsatkueishanislandhydrothermalventfieldtaiwan
AT shengyuguo growthstudyundercombinedeffectsoftemperaturephandsalinityandtranscriptomeanalysisrevealedadaptationsofaspergillusterreusntou4989totheextremeconditionsatkueishanislandhydrothermalventfieldtaiwan
AT chiyushih growthstudyundercombinedeffectsoftemperaturephandsalinityandtranscriptomeanalysisrevealedadaptationsofaspergillusterreusntou4989totheextremeconditionsatkueishanislandhydrothermalventfieldtaiwan
AT hansudahms growthstudyundercombinedeffectsoftemperaturephandsalinityandtranscriptomeanalysisrevealedadaptationsofaspergillusterreusntou4989totheextremeconditionsatkueishanislandhydrothermalventfieldtaiwan
AT jiangshiouhwang growthstudyundercombinedeffectsoftemperaturephandsalinityandtranscriptomeanalysisrevealedadaptationsofaspergillusterreusntou4989totheextremeconditionsatkueishanislandhydrothermalventfieldtaiwan
AT hyojungcha growthstudyundercombinedeffectsoftemperaturephandsalinityandtranscriptomeanalysisrevealedadaptationsofaspergillusterreusntou4989totheextremeconditionsatkueishanislandhydrothermalventfieldtaiwan
_version_ 1714814976509607936