DOI: 10.1111/j.1550-7408.1997.tb05946.x. Germination of Nosema algerae (Microspora) Spores: Conditional Inhibition by D2O, Ethanol and Hg2+ Suggests Dependence of Water Influx upon Membrane Hydration and Specific Transmembrane Pathways

Germination of Nosema algerae (Microspora) Spores: Conditional Inhibition by D2O, Ethanol and Hg2+ Suggests Dependence of Water Influx upon Membrane Hydration and Specific Transmembrane Pathways

10.1111/j.1550-7408.1997.tb05946.x

Crossref journal-article

Wiley

Journal of Eukaryotic Microbiology (311)

Abstract

ABSTRACT. The germination of microsporidian spores under conditions expected to affect water flow across the plasma membrane‐wall complex was studied by assessing their responses to in vitro stimulation with Na+ or K+. Partial or full substitution of common water with D2O, which more effectively coats ions and electrostatically‐charged cell surfaces with relatively stable hydration layers, delayed and inhibited spore germination in a concentration‐dependent manner; yet, preincubation in 100% D2O did not change the normal response to standard stimulation. Water structure‐breaking conditions, such as an increase in temperature (within the 15° C to 40° C range) or in ionic strength (2‐ to 10‐fold normal), opposed the inhibition by D2O and allowed significant stimulation by Li+, the monovalent cation with the largest hydration diameter and a usually weak stimulant action on the spores. Ethanol, known to reduce water permeation across cell membranes and phospholipid bilayers, also caused a powerful and dose‐dependent (1% to 4% v/v) inhibition of spore germination, but pretreatment with ethanol did not affect the normal response. HgCl2, an inhibitor of specific water channels, blocked spore germination at just 250 μM in the normal stimulation solution irrespective of the temperature, and permitted only a delayed response in high salt stimulation solutions. However, the inhibition by Hg2+ was abolished by the simultaneous presence of 2‐mercaptoethanol in the medium. These results suggest (1) that spore germination is keenly dependent upon the hydration states of both the plasma membrane‐wall complex and the stimulant ions, and (2) that osmotic water flows into the spores through specific transmembrane pathways with critical sulfhydryl groups, i.e. analogous to the water channels that facilitate water movements across the plasma membranes of highly permeable cells.

Bibliography

FRIXIONE, E., RUIZ, L., CERBÃN, J., & UNDEEN, A. H. (1997). Germination of Nosema algerae (Microspora) Spores: Conditional Inhibition by D2O, Ethanol and Hg2+ Suggests Dependence of Water Influx upon Membrane Hydration and Specific Transmembrane Pathways. Journal of Eukaryotic Microbiology, 44(2), 109â116. Portico.

Authors 4

EUGENIO FRIXIONE (first)
LOURDES RUIZ (additional)
JORGE CERBÓN (additional)
ALBERT H. UNDEEN (additional)

References 48 Referenced 61

{'key': 'e_1_2_1_2_2', 'first-page': 'F463', 'article-title': 'Aquaporin CHIP: the archetypal molecular water channel', 'volume': '256', 'author': 'Agre P.', 'year': '1993', 'journal-title': 'Am. J. Physiol'} / Am. J. Physiol / Aquaporin CHIP: the archetypal molecular water channel by Agre P. (1993)
10.1016/0006-8993(72)90301-0
10.1007/BF00233382
{'key': 'e_1_2_1_5_2', 'first-page': '123', 'article-title': 'The role of protons in nerve conduction', 'volume': '115', 'author': 'Bass L.', 'year': '1973', 'journal-title': 'Progr, Biophys. Mol. Biol'} / Progr, Biophys. Mol. Biol / The role of protons in nerve conduction by Bass L. (1973)
10.1111/j.1550-7408.1993.tb04889.x
10.1016/0005-2760(67)90071-9
10.1016/0005-2736(70)90244-0
10.1016/0022-5193(83)90225-4
10.1006/jipa.1993.1103
10.1111/j.1471-4159.1971.tb00022.x
10.1016/S0959-440X(94)90217-8
10.1016/0022-2011(69)90162-1
10.1002/neu.480100606
10.1111/j.1550-7408.1994.tb06043.x
10.1002/cm.970220105
10.1111/j.1749-6632.1960.tb39106.x
10.1139/m67-178
10.1016/S0006-3495(95)80275-4
{'key': 'e_1_2_1_20_2', 'first-page': '190', 'volume-title': 'Structure and Function of Biological Membranes', 'author': 'Kavanau J. L.', 'year': '1965'} / Structure and Function of Biological Membranes by Kavanau J. L. (1965)
10.1016/0005-2736(95)80033-C
10.1016/0040-8166(75)90030-0
10.1111/j.1550-7408.1973.tb03586.x
{'key': 'e_1_2_1_24_2', 'first-page': '81', 'article-title': 'The mode of sporoplasm extrusion in microsporidian spores', 'volume': '1', 'author': 'Lom J.', 'year': '1963', 'journal-title': 'Acta Protozool'} / Acta Protozool / The mode of sporoplasm extrusion in microsporidian spores by Lom J. (1963)
10.1016/0005-2736(70)90130-6
10.1002/jcp.1040700211
10.1002/jcp.1040770209
10.1111/j.1365-2958.1991.tb01823.x
10.1126/science.256.5055.385
10.1016/S0021-9258(18)54108-9 / J. Biol. Chem / The mercury‐sensitive residue at cysteine‐189 in the CHIP28 wate channel by Preston G. M. (1993)
10.1111/j.1749-6632.1960.tb39094.x
{'key': 'e_1_2_1_32_2', 'first-page': '14', 'volume-title': 'Comparative Pathobiology, Vol. 2. Systematics of the Microsporidia', 'author': 'Sprague V.', 'year': '1977'} / Comparative Pathobiology, Vol. 2. Systematics of the Microsporidia by Sprague V. (1977)
{'key': 'e_1_2_1_33_2', 'first-page': '29', 'article-title': 'Spore‐hatching processes in some Nosema species, with particular reference to N. algerae Vávra and Undeen', 'volume': '11', 'author': 'Undeen A. H.', 'year': '1978', 'journal-title': 'Mics. Publ. Entomol. Soc. Am'} / Mics. Publ. Entomol. Soc. Am / Spore‐hatching processes in some Nosema species, with particular reference to N. algerae Vávra and Undeen by Undeen A. H. (1978)
10.1111/j.1550-7408.1983.tb02915.x
10.1016/S0022-5193(05)80223-1
10.1016/0022-2011(83)90184-2
10.1016/0022-2011(88)90106-1
10.1016/0022-2011(88)90133-4
10.1016/0022-2011(88)90142-5
10.1016/0022-2011(87)90087-5
10.1111/j.1550-7408.1990.tb01265.x
10.1111/j.1550-7408.1991.tb04826.x
10.1111/j.1550-7408.1994.tb01485.x
{'key': 'e_1_2_1_44_2', 'first-page': '49', 'article-title': 'Hydrolyse enzimatique des spores des microsporides', 'volume': '14', 'author': 'Vávra J.', 'year': '1967', 'journal-title': 'J. Protozool'} / J. Protozool / Hydrolyse enzimatique des spores des microsporides by Vávra J. (1967)
{'key': 'e_1_2_1_45_2', 'first-page': '1', 'volume-title': 'Comparative Pathobiology, Vol. I. Biology of the Microsporidia', 'author': 'Vávra J.', 'year': '1977'} / Comparative Pathobiology, Vol. I. Biology of the Microsporidia by Vávra J. (1977)
{'key': 'e_1_2_1_46_2', 'first-page': '143', 'article-title': 'A freeze‐fracture study of microsporidia (Protozoa: Microspora). I. The sporophorous vesicel, the spore wall, and the spore plasma membrane', 'volume': '122', 'author': 'Vávra J.', 'year': '1986', 'journal-title': 'Protistologica'} / Protistologica / A freeze‐fracture study of microsporidia (Protozoa: Microspora). I. The sporophorous vesicel, the spore wall, and the spore plasma membrane by Vávra J. (1986)
10.1083/jcb.123.3.605
10.2307/1542078
10.1021/bi00172a042

Dates

Type	When
Created	18 years, 3 months ago (May 14, 2007, 1:58 a.m.)
Deposited	1 year, 9 months ago (Oct. 27, 2023, 12:39 p.m.)
Indexed	3 weeks, 6 days ago (July 27, 2025, 3:55 a.m.)
Issued	28 years, 5 months ago (March 1, 1997)
Published	28 years, 5 months ago (March 1, 1997)
Published Online	18 years, 3 months ago (May 1, 2007)
Published Print	28 years, 5 months ago (March 1, 1997)

Funders 0

None

BibTeX

@article{FRIXIONE_1997, title={Germination of Nosema algerae (Microspora) Spores: Conditional Inhibition by D2O, Ethanol and Hg2+ Suggests Dependence of Water Influx upon Membrane Hydration and Specific Transmembrane Pathways}, volume={44}, ISSN={1550-7408}, url={http://dx.doi.org/10.1111/j.1550-7408.1997.tb05946.x}, DOI={10.1111/j.1550-7408.1997.tb05946.x}, number={2}, journal={Journal of Eukaryotic Microbiology}, publisher={Wiley}, author={FRIXIONE, EUGENIO and RUIZ, LOURDES and CERBÓN, JORGE and UNDEEN, ALBERT H.}, year={1997}, month=mar, pages={109–116} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        27
      ]
    ],
    "date-time": "2025-07-27T07:55:25Z",
    "timestamp": 1753602925109
  },
  "reference-count": 48,
  "publisher": "Wiley",
  "issue": "2",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2007,
            5,
            1
          ]
        ],
        "date-time": "2007-05-01T00:00:00Z",
        "timestamp": 1177977600000
      },
      "content-version": "vor",
      "delay-in-days": 3713,
      "URL": "http://onlinelibrary.wiley.com/termsAndConditions#vor"
    }
  ],
  "content-domain": {
    "domain": [
      "onlinelibrary.wiley.com"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        1997,
        3
      ]
    ]
  },
  "abstract": "<jats:p><jats:bold>ABSTRACT. </jats:bold> The germination of microsporidian spores under conditions expected to affect water flow across the plasma membrane\u2010wall complex was studied by assessing their responses to in vitro stimulation with Na<jats:sup>+</jats:sup> or K<jats:sup>+</jats:sup>. Partial or full substitution of common water with D<jats:sub>2</jats:sub>O, which more effectively coats ions and electrostatically\u2010charged cell surfaces with relatively stable hydration layers, delayed and inhibited spore germination in a concentration\u2010dependent manner; yet, preincubation in 100% D<jats:sub>2</jats:sub>O did not change the normal response to standard stimulation. Water structure\u2010breaking conditions, such as an increase in temperature (within the 15\u00b0 C to 40\u00b0 C range) or in ionic strength (2\u2010 to 10\u2010fold normal), opposed the inhibition by D<jats:sub>2</jats:sub>O and allowed significant stimulation by Li<jats:sup>+</jats:sup>, the monovalent cation with the largest hydration diameter and a usually weak stimulant action on the spores. Ethanol, known to reduce water permeation across cell membranes and phospholipid bilayers, also caused a powerful and dose\u2010dependent (1% to 4% v/v) inhibition of spore germination, but pretreatment with ethanol did not affect the normal response. HgCl<jats:sub>2</jats:sub>, an inhibitor of specific water channels, blocked spore germination at just 250 \u03bcM in the normal stimulation solution irrespective of the temperature, and permitted only a delayed response in high salt stimulation solutions. However, the inhibition by Hg<jats:sup>2+</jats:sup> was abolished by the simultaneous presence of 2\u2010mercaptoethanol in the medium. These results suggest (1) that spore germination is keenly dependent upon the hydration states of both the plasma membrane\u2010wall complex and the stimulant ions, and (2) that osmotic water flows into the spores through specific transmembrane pathways with critical sulfhydryl groups, i.e. analogous to the water channels that facilitate water movements across the plasma membranes of highly permeable cells.</jats:p>",
  "DOI": "10.1111/j.1550-7408.1997.tb05946.x",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2007,
        5,
        14
      ]
    ],
    "date-time": "2007-05-14T05:58:46Z",
    "timestamp": 1179122326000
  },
  "page": "109-116",
  "update-policy": "http://dx.doi.org/10.1002/crossmark_policy",
  "source": "Crossref",
  "is-referenced-by-count": 61,
  "title": "Germination of <i>Nosema algerae</i> (Microspora) Spores: Conditional Inhibition by D<sub>2</sub>O, Ethanol and Hg<sup>2+</sup> Suggests Dependence of Water Influx upon Membrane Hydration and Specific Transmembrane Pathways",
  "prefix": "10.1111",
  "volume": "44",
  "author": [
    {
      "given": "EUGENIO",
      "family": "FRIXIONE",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "LOURDES",
      "family": "RUIZ",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "JORGE",
      "family": "CERB\u00d3N",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "ALBERT H.",
      "family": "UNDEEN",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "311",
  "published-online": {
    "date-parts": [
      [
        2007,
        5
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_2_1_2_2",
      "first-page": "F463",
      "article-title": "Aquaporin CHIP: the archetypal molecular water channel",
      "volume": "256",
      "author": "Agre P.",
      "year": "1993",
      "journal-title": "Am. J. Physiol"
    },
    {
      "key": "e_1_2_1_3_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(72)90301-0"
    },
    {
      "key": "e_1_2_1_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00233382"
    },
    {
      "key": "e_1_2_1_5_2",
      "first-page": "123",
      "article-title": "The role of protons in nerve conduction",
      "volume": "115",
      "author": "Bass L.",
      "year": "1973",
      "journal-title": "Progr, Biophys. Mol. Biol"
    },
    {
      "key": "e_1_2_1_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1550-7408.1993.tb04889.x"
    },
    {
      "key": "e_1_2_1_7_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0005-2760(67)90071-9"
    },
    {
      "key": "e_1_2_1_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0005-2736(70)90244-0"
    },
    {
      "key": "e_1_2_1_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-5193(83)90225-4"
    },
    {
      "key": "e_1_2_1_10_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/jipa.1993.1103"
    },
    {
      "key": "e_1_2_1_11_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1471-4159.1971.tb00022.x"
    },
    {
      "key": "e_1_2_1_12_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0959-440X(94)90217-8"
    },
    {
      "key": "e_1_2_1_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-2011(69)90162-1"
    },
    {
      "key": "e_1_2_1_14_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/neu.480100606"
    },
    {
      "key": "e_1_2_1_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1550-7408.1994.tb06043.x"
    },
    {
      "key": "e_1_2_1_16_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cm.970220105"
    },
    {
      "key": "e_1_2_1_17_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1749-6632.1960.tb39106.x"
    },
    {
      "key": "e_1_2_1_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1139/m67-178"
    },
    {
      "key": "e_1_2_1_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0006-3495(95)80275-4"
    },
    {
      "key": "e_1_2_1_20_2",
      "first-page": "190",
      "volume-title": "Structure and Function of Biological Membranes",
      "author": "Kavanau J. L.",
      "year": "1965"
    },
    {
      "key": "e_1_2_1_21_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0005-2736(95)80033-C"
    },
    {
      "key": "e_1_2_1_22_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0040-8166(75)90030-0"
    },
    {
      "key": "e_1_2_1_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1550-7408.1973.tb03586.x"
    },
    {
      "key": "e_1_2_1_24_2",
      "first-page": "81",
      "article-title": "The mode of sporoplasm extrusion in microsporidian spores",
      "volume": "1",
      "author": "Lom J.",
      "year": "1963",
      "journal-title": "Acta Protozool"
    },
    {
      "key": "e_1_2_1_25_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0005-2736(70)90130-6"
    },
    {
      "key": "e_1_2_1_26_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jcp.1040700211"
    },
    {
      "key": "e_1_2_1_27_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jcp.1040770209"
    },
    {
      "key": "e_1_2_1_28_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1365-2958.1991.tb01823.x"
    },
    {
      "key": "e_1_2_1_29_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.256.5055.385"
    },
    {
      "key": "e_1_2_1_30_2",
      "doi-asserted-by": "crossref",
      "first-page": "17",
      "DOI": "10.1016/S0021-9258(18)54108-9",
      "article-title": "The mercury\u2010sensitive residue at cysteine\u2010189 in the CHIP28 wate channel",
      "volume": "268",
      "author": "Preston G. M.",
      "year": "1993",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "e_1_2_1_31_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1749-6632.1960.tb39094.x"
    },
    {
      "key": "e_1_2_1_32_2",
      "first-page": "14",
      "volume-title": "Comparative Pathobiology, Vol. 2. Systematics of the Microsporidia",
      "author": "Sprague V.",
      "year": "1977"
    },
    {
      "key": "e_1_2_1_33_2",
      "first-page": "29",
      "article-title": "Spore\u2010hatching processes in some Nosema species, with particular reference to N. algerae V\u00e1vra and Undeen",
      "volume": "11",
      "author": "Undeen A. H.",
      "year": "1978",
      "journal-title": "Mics. Publ. Entomol. Soc. Am"
    },
    {
      "key": "e_1_2_1_34_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1550-7408.1983.tb02915.x"
    },
    {
      "key": "e_1_2_1_35_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0022-5193(05)80223-1"
    },
    {
      "key": "e_1_2_1_36_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-2011(83)90184-2"
    },
    {
      "key": "e_1_2_1_37_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-2011(88)90106-1"
    },
    {
      "key": "e_1_2_1_38_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-2011(88)90133-4"
    },
    {
      "key": "e_1_2_1_39_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-2011(88)90142-5"
    },
    {
      "key": "e_1_2_1_40_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-2011(87)90087-5"
    },
    {
      "key": "e_1_2_1_41_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1550-7408.1990.tb01265.x"
    },
    {
      "key": "e_1_2_1_42_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1550-7408.1991.tb04826.x"
    },
    {
      "key": "e_1_2_1_43_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1550-7408.1994.tb01485.x"
    },
    {
      "key": "e_1_2_1_44_2",
      "first-page": "49",
      "article-title": "Hydrolyse enzimatique des spores des microsporides",
      "volume": "14",
      "author": "V\u00e1vra J.",
      "year": "1967",
      "journal-title": "J. Protozool"
    },
    {
      "key": "e_1_2_1_45_2",
      "first-page": "1",
      "volume-title": "Comparative Pathobiology, Vol. I. Biology of the Microsporidia",
      "author": "V\u00e1vra J.",
      "year": "1977"
    },
    {
      "key": "e_1_2_1_46_2",
      "first-page": "143",
      "article-title": "A freeze\u2010fracture study of microsporidia (Protozoa: Microspora). I. The sporophorous vesicel, the spore wall, and the spore plasma membrane",
      "volume": "122",
      "author": "V\u00e1vra J.",
      "year": "1986",
      "journal-title": "Protistologica"
    },
    {
      "key": "e_1_2_1_47_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.123.3.605"
    },
    {
      "key": "e_1_2_1_48_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.2307/1542078"
    },
    {
      "key": "e_1_2_1_49_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00172a042"
    }
  ],
  "container-title": "Journal of Eukaryotic Microbiology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1111%2Fj.1550-7408.1997.tb05946.x",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1550-7408.1997.tb05946.x",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        10,
        27
      ]
    ],
    "date-time": "2023-10-27T16:39:05Z",
    "timestamp": 1698424745000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://onlinelibrary.wiley.com/doi/10.1111/j.1550-7408.1997.tb05946.x"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1997,
        3
      ]
    ]
  },
  "references-count": 48,
  "journal-issue": {
    "issue": "2",
    "published-print": {
      "date-parts": [
        [
          1997,
          3
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1111/j.1550-7408.1997.tb05946.x"
  ],
  "URL": "http://dx.doi.org/10.1111/j.1550-7408.1997.tb05946.x",
  "relation": {},
  "ISSN": [
    "1066-5234",
    "1550-7408"
  ],
  "subject": [],
  "container-title-short": "J Eukaryotic Microbiology",
  "published": {
    "date-parts": [
      [
        1997,
        3
      ]
    ]
  },
  "assertion": [
    {
      "value": "2007-05-01",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}