Register      Login
Soil Research Soil Research Society
Soil, land care and environmental research
RESEARCH ARTICLE

Altitudinal transects reveal large differences in intact lipid composition among soils

Charles R. Warren https://orcid.org/0000-0002-0788-4713
+ Author Affiliations
- Author Affiliations

School of Life and Environmental Sciences, Heydon-Laurence Building A08, University of Sydney, NSW 2006, Australia. Email: charles.warren@sydney.edu.au

Soil Research - https://doi.org/10.1071/SR20055
Submitted: 27 February 2020  Accepted: 29 January 2021   Published online: 18 March 2021

Abstract

Fatty acid-based lipids comprise a small but important component of soil organic matter. Lipids are indispensable components of soil microbes due to their function as components of membranes and as stores of energy and C. Hence, lipid composition is likely under strong selection pressure and there ought to be strong associations between lipid composition of microbial communities and environmental conditions. Associations between microbial lipids and environment likely involve an integrated combination of differences in lipid headgroups (classes) and fatty acyl chains. However, past studies examining associations between soil lipid composition and environmental conditions have focussed on fatty acids hydrolysed from polar lipids and less is known about headgroups (classes) of polar lipids. The aim of this study was to examine associations between environmental conditions changing with altitude and the intact polar and non-polar lipids of soil microbial communities. We used two altitudinal transects, both spanning from forest through to above the alpine treeline, but separated from one another by ~700 km. Liquid chromatography-mass spectrometry identified 174 intact lipids to the level of class and sum composition. Approximately half of the pool of fatty acid-based lipids was accounted for by two classes of non-polar lipids (diacylglycerol and triacylglycerols), while the other half was dominated by three classes of polar lipids (phosphatidylethanolamine, phosphatidylcholine and diacylglyceryl-N,N,N-trimethylhomoserine). There were large differences among sites in the relative amounts of lipid classes. For example, diacylglyceryl-N,N,N-trimethylhomoserine varied among sites from 5 to 41% of the polar lipid pool, phosphatidylcholine from 31 to 60% of the polar lipid pool, and diacylglycerols from 9 to 53% of the total non-polar pool. Relationships of lipid composition with altitude were weak or differed between transects, and pH was the variable most strongly associated with lipid composition. Variation among sites in the relative abundance of phosphatidylcholine were positively associated with pH, while relative and absolute abundance of diacylglycerol was negatively related to pH. We suggest that the accumulation of diacylglycerol at low pH represents slowed hydrolysis and/or microbial utilisation. A large fraction of variance among sites in lipid composition remained unexplained, which highlights the need for additional research on processes leading to production and consumption of fatty acid-based lipids.

Keywords: altitude, betaine lipid, LC/MS, lipid, microbial biomass, phospholipid, temperature, environmental conditions, microbial communities, fatty acid inventory, pH.


References

Alvarez H, Steinbüchel A (2002) Triacylglycerols in prokaryotic microorganisms. Applied Microbiology and Biotechnology 60, 367–376.
Triacylglycerols in prokaryotic microorganisms.Crossref | GoogleScholarGoogle Scholar | 12466875PubMed |

Álvarez AM, Carral P, Hernández Z, Almendros G (2016) Hydrocarbon pollution from domestic oil recycling industries in peri-urban soils. Lipid molecular assemblages. Journal of Environmental Chemical Engineering 4, 695–703.
Hydrocarbon pollution from domestic oil recycling industries in peri-urban soils. Lipid molecular assemblages.Crossref | GoogleScholarGoogle Scholar |

Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46.
A new method for non-parametric multivariate analysis of variance.Crossref | GoogleScholarGoogle Scholar |

Assis CPd, González-Vila FJ, Jucksch I, González-Pérez JA, Neves JCL, Lani JL, Mendonça EDS (2011) Lipid abundance and composition of a humic Oxisol as a function of land use. Scientia Agricola 68, 230–236.
Lipid abundance and composition of a humic Oxisol as a function of land use.Crossref | GoogleScholarGoogle Scholar |

Bååth E (2003) The use of neutral lipid fatty acids to indicate the physiological conditions of soil fungi. Microbial Ecology 45, 373–383.
The use of neutral lipid fatty acids to indicate the physiological conditions of soil fungi.Crossref | GoogleScholarGoogle Scholar | 12704558PubMed |

Bååth E, Anderson TH (2003) Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biology & Biochemistry 35, 955–963.
Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques.Crossref | GoogleScholarGoogle Scholar |

Bago B, Zipfel W, Williams RM, Jun J, Arreola R, Lammers PJ, Pfeffer PE, Shachar-Hill Y (2002) Translocation and utilization of fungal storage lipid in the arbuscular mycorrhizal symbiosis. Plant Physiology 128, 108–124.
Translocation and utilization of fungal storage lipid in the arbuscular mycorrhizal symbiosis.Crossref | GoogleScholarGoogle Scholar | 11788757PubMed |

Benning C, Huang ZH, Gage DA (1995) Accumulation of a novel glycolipid and a betaine lipid in cells of Rhodobacter sphaeroides grown under phosphate limitation. Archives of Biochemistry and Biophysics 317, 103–111.
Accumulation of a novel glycolipid and a betaine lipid in cells of Rhodobacter sphaeroides grown under phosphate limitation.Crossref | GoogleScholarGoogle Scholar | 7872771PubMed |

Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37, 911–917.
A rapid method of total lipid extraction and purification.Crossref | GoogleScholarGoogle Scholar | 13671378PubMed |

Bull ID, van Bergen PFR, Poulton P, Evershed RP (1998) Organic geochemical studies of soils from the Rothamsted Classical Experiments—II, Soils from the Hoosfield Spring Barley Experiment treated with different quantities of manure. Organic Geochemistry 28, 11–26.
Organic geochemical studies of soils from the Rothamsted Classical Experiments—II, Soils from the Hoosfield Spring Barley Experiment treated with different quantities of manure.Crossref | GoogleScholarGoogle Scholar |

Buyer JS, Sasser M (2012) High throughput phospholipid fatty acid analysis of soils. Applied Soil Ecology 61, 127–130.
High throughput phospholipid fatty acid analysis of soils.Crossref | GoogleScholarGoogle Scholar |

Cullis PR, Fenske DB, Hope MJ (1996) Physical properties and functional roles of lipids in membranes. In ‘Physical properties and functional roles of lipids in membranes. New Comprehensive Biochemistry’ Vol. 31. (Eds DE Vance, JE Vance.) pp. 1–33. (Elsevier: Amsterdam)

DeBell RM, Jack RC (1975) Stereospecific analysis of major glycerolipids of Phycomyces blakesleeanus sporangiophores and mycelium. Journal of Bacteriology 124, 220–224.
Stereospecific analysis of major glycerolipids of Phycomyces blakesleeanus sporangiophores and mycelium.Crossref | GoogleScholarGoogle Scholar | 1176431PubMed |

Delgado-Baquerizo M, Fry EL, Eldridge DJ, de Vries FT, Manning P, Hamonts K, Kattge J, Boenisch G, Singh BK, Bardgett RD (2018) Plant attributes explain the distribution of soil microbial communities in two contrasting regions of the globe. New Phytologist 219, 574–587.
Plant attributes explain the distribution of soil microbial communities in two contrasting regions of the globe.Crossref | GoogleScholarGoogle Scholar |

Dinel H, Schnitzer M, Mehuys GR (1990) Soil lipids: origin, nature, content, decomposition and effect on soil physical properties. In ‘Soil Biochemistry, Vol 6’. (Eds J-M Bollag, G Stotzky.) pp. 397–429. (Marcel Dekker: New York)

Dippold MA, Kuzyakov Y (2016) Direct incorporation of fatty acids into microbial phospholipids in soils: Position-specific labeling tells the story. Geochimica et Cosmochimica Acta 174, 211–221.
Direct incorporation of fatty acids into microbial phospholipids in soils: Position-specific labeling tells the story.Crossref | GoogleScholarGoogle Scholar |

Doolette AL, Smernik RJ, McLaren TI (2017) The composition of organic phosphorus in soils of the Snowy Mountains region of south-eastern Australia. Soil Research 55, 10–18.
The composition of organic phosphorus in soils of the Snowy Mountains region of south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |

Dörmann P, Benning C (2002) Galactolipids rule in seed plants. Trends in Plant Science 7, 112–118.
Galactolipids rule in seed plants.Crossref | GoogleScholarGoogle Scholar | 11906834PubMed |

Evans SE, Wallenstein MD (2014) Climate change alters ecological strategies of soil bacteria. Ecology Letters 17, 155–164.
Climate change alters ecological strategies of soil bacteria.Crossref | GoogleScholarGoogle Scholar | 24261594PubMed |

Fierer N, McCain CM, Meir P, Zimmermann M, Rapp JM, Silman MR, Knight R (2011) Microbes do not follow the elevational diversity patterns of plants and animals. Ecology 92, 797–804.
Microbes do not follow the elevational diversity patterns of plants and animals.Crossref | GoogleScholarGoogle Scholar | 21661542PubMed |

Findlay RH, King GM, Watling L (1989) Efficacy of phospholipid analysis in determining microbial biomass in sediments. Applied and Environmental Microbiology 55, 2888–2893.
Efficacy of phospholipid analysis in determining microbial biomass in sediments.Crossref | GoogleScholarGoogle Scholar | 16348051PubMed |

Frostegård A, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biology and Fertility of Soils 22, 59–65.
The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil.Crossref | GoogleScholarGoogle Scholar |

Frostegård A, Tunlid A, Bååth E (1991) Microbial biomass measured as total lipid phosphate in soils of different organic content. Journal of Microbiological Methods 14, 151–163.
Microbial biomass measured as total lipid phosphate in soils of different organic content.Crossref | GoogleScholarGoogle Scholar |

Frostegård A, Tunlid A, Bååth E (2011) Use and misuse of PLFA measurements in soils. Soil Biology & Biochemistry 43, 1621–1625.
Use and misuse of PLFA measurements in soils.Crossref | GoogleScholarGoogle Scholar |

Haack SK, Garchow H, Odelson DA, Forney LJ, Klug MJ (1994) Accuracy, reproducibility, and interpretation of fatty-acid methyl-ester profiles of model bacterial communities. Applied and Environmental Microbiology 60, 2483–2493.
Accuracy, reproducibility, and interpretation of fatty-acid methyl-ester profiles of model bacterial communities.Crossref | GoogleScholarGoogle Scholar | 16349327PubMed |

Hammer Ø, Harper D, Ryan P (2001) PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4, 1–9.

Harwood JL (1980) Plant acyl lipids: structure, distribution and analysis. In ‘The Biochemistry of Plants. Vol. 4. Lipids: Structure and Function’. (Ed. PK Stumpf.) pp. 1–55. (Academic Press: New York)

Harwood JL, Russell NJ (1984) ‘Lipids in plants and microbes.’ (George Allen & Unwin Ltd: London)

Hobbie SE, Schimel JP, Trumbore SE, Randerson JR (2000) Controls over carbon storage and turnover in high-latitude soils. Global Change Biology 6, 196–210.
Controls over carbon storage and turnover in high-latitude soils.Crossref | GoogleScholarGoogle Scholar |

Jackson FM, Michaelson L, Fraser TC, Stobart AK, Griffiths G (1998) Biosynthesis of triacylglycerol in the filamentous fungus Mucor circinelloides. Microbiology 144, 2639–2645.
Biosynthesis of triacylglycerol in the filamentous fungus Mucor circinelloides.Crossref | GoogleScholarGoogle Scholar | 9782513PubMed |

Joergensen RG, Wichern F (2008) Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biology & Biochemistry 40, 2977–2991.
Quantitative assessment of the fungal contribution to microbial tissue in soil.Crossref | GoogleScholarGoogle Scholar |

Jones DL, Cooledge EC, Hoyle FC, Griffiths RI, Murphy DV (2019) pH and exchangeable aluminum are major regulators of microbial energy flow and carbon use efficiency in soil microbial communities. Soil Biology & Biochemistry 138, 107584
pH and exchangeable aluminum are major regulators of microbial energy flow and carbon use efficiency in soil microbial communities.Crossref | GoogleScholarGoogle Scholar |

Kaup MT, Froese CD, Thompson JE (2002) A role for diacylglycerol acyltransferase during leaf senescence. Plant Physiology 129, 1616–1626.
A role for diacylglycerol acyltransferase during leaf senescence.Crossref | GoogleScholarGoogle Scholar | 12177474PubMed |

Kendrick A, Ratledge C (1992) Phospholipid fatty acyl distribution of three fungi indicates positional specificity for n-6vs. n-3 fatty acids. Lipids 27, 505–508.
Phospholipid fatty acyl distribution of three fungi indicates positional specificity for n-6vs. n-3 fatty acids.Crossref | GoogleScholarGoogle Scholar |

Körner C (2007) The use of ‘altitude’ in ecological research. Trends in Ecology & Evolution 22, 569–574.
The use of ‘altitude’ in ecological research.Crossref | GoogleScholarGoogle Scholar |

Kotas P, Šantrůčková H, Elster J, Kaštovská E (2018) Soil microbial biomass, activity and community composition along altitudinal gradients in the High Arctic (Billefjorden, Svalbard). Biogeosciences 15, 1879–1894.
Soil microbial biomass, activity and community composition along altitudinal gradients in the High Arctic (Billefjorden, Svalbard).Crossref | GoogleScholarGoogle Scholar |

Kuzyakov Y, Bogomolova I, Glaser B (2014) Biochar stability in soil: Decomposition during eight years and transformation as assessed by compound-specific C-14 analysis. Soil Biology & Biochemistry 70, 229–236.
Biochar stability in soil: Decomposition during eight years and transformation as assessed by compound-specific C-14 analysis.Crossref | GoogleScholarGoogle Scholar |

Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends in Ecology & Evolution 23, 95–103.
Plant nutrient-acquisition strategies change with soil age.Crossref | GoogleScholarGoogle Scholar |

Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biology & Biochemistry 40, 2407–2415.
The influence of soil properties on the structure of bacterial and fungal communities across land-use types.Crossref | GoogleScholarGoogle Scholar |

Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-Based Assessment of Soil pH as a Predictor of Soil Bacterial Community Structure at the Continental Scale. Applied and Environmental Microbiology 75, 5111–5120.
Pyrosequencing-Based Assessment of Soil pH as a Predictor of Soil Bacterial Community Structure at the Continental Scale.Crossref | GoogleScholarGoogle Scholar | 19502440PubMed |

Lin YT, Whitman WB, Coleman DC, Shi SY, Tang SL, Chiu CY (2015) Changes of soil bacterial communities in bamboo plantations at different elevations. FEMS Microbiology Ecology 91,
Changes of soil bacterial communities in bamboo plantations at different elevations.Crossref | GoogleScholarGoogle Scholar | 25873459PubMed |

Liu XL, Leider A, Gillespie A, Groger J, Versteegh GJM, Hinrichs KU (2010) Identification of polar lipid precursors of the ubiquitous branched GDGT orphan lipids in a peat bog in Northern Germany. Organic Geochemistry 41, 653–660.
Identification of polar lipid precursors of the ubiquitous branched GDGT orphan lipids in a peat bog in Northern Germany.Crossref | GoogleScholarGoogle Scholar |

Maggi O, Tosi S, Angelova M, Lagostina E, Fabbri AA, Pecoraro L, Altobelli E, Picco AM, Savino E, Branda E, Turchetti B, Zotti M, Vizzini A, Buzzini P (2013) Adaptation of fungi, including yeasts, to cold environments. Plant Biosystems - An International Journal Dealing with all Aspects of Plant Biology 147, 247–258.
Adaptation of fungi, including yeasts, to cold environments.Crossref | GoogleScholarGoogle Scholar |

Malik AA, Puissant J, Buckeridge KM, Goodall T, Jehmlich N, Chowdhury S, Gweon HS, Peyton JM, Mason KE, van Agtmaal M, Blaud A, Clark IM, Whitaker J, Pywell RF, Ostle N, Gleixner G, Griffiths RI (2018) Land use driven change in soil pH affects microbial carbon cycling processes. Nature Communications 9, 3591
Land use driven change in soil pH affects microbial carbon cycling processes.Crossref | GoogleScholarGoogle Scholar | 30181597PubMed |

Malosso E, English L, Hopkins DW, O’Donnell AG (2004) Use of C-13-labelled plant materials and ergosterol, PLFA and NLFA analyses to investigate organic matter decomposition in Antarctic soil. Soil Biology & Biochemistry 36, 165–175.
Use of C-13-labelled plant materials and ergosterol, PLFA and NLFA analyses to investigate organic matter decomposition in Antarctic soil.Crossref | GoogleScholarGoogle Scholar |

Mangelsdorf K, Finsel E, Liebner S, Wagner D (2009) Temperature adaptation of microbial communities in different horizons of Siberian permafrost-affected soils from the Lena Delta. Geochemistry 69, 169–182.
Temperature adaptation of microbial communities in different horizons of Siberian permafrost-affected soils from the Lena Delta.Crossref | GoogleScholarGoogle Scholar |

Margesin R, Jud M, Tscherko D, Schinner F (2009) Microbial communities and activities in alpine and subalpine soils. FEMS Microbiology Ecology 67, 208–218.
Microbial communities and activities in alpine and subalpine soils.Crossref | GoogleScholarGoogle Scholar | 19049494PubMed |

Massaccesi L, De Feudis M, Leccese A, Agnelli A (2020) Altitude and Vegetation Affect Soil Organic Carbon, Basal Respiration and Microbial Biomass in Apennine Forest Soils. Forests 11, 710
Altitude and Vegetation Affect Soil Organic Carbon, Basal Respiration and Microbial Biomass in Apennine Forest Soils.Crossref | GoogleScholarGoogle Scholar |

Meng H, Li K, Nie M, Wan JR, Quan ZX, Fang CM, Chen JK, Gu JD, Li B (2013) Responses of bacterial and fungal communities to an elevation gradient in a subtropical montane forest of China. Applied Microbiology and Biotechnology 97, 2219–2230.
Responses of bacterial and fungal communities to an elevation gradient in a subtropical montane forest of China.Crossref | GoogleScholarGoogle Scholar | 22539023PubMed |

Mercado I, García‐Calderón N, Ibáñez A, Martin F (2000) Composition of soil lipids in two chinampas agroecosystems from Xochimilco and Tlahuac municipalities, Mexico. Communications in Soil Science and Plant Analysis 31, 1003–1016.
Composition of soil lipids in two chinampas agroecosystems from Xochimilco and Tlahuac municipalities, Mexico.Crossref | GoogleScholarGoogle Scholar |

Motavalli PP, Palm CA, Parton WJ, Elliott ET, Frey SD (1995) Soil pH and organic C dynamics in tropical forest soils: Evidence from laboratory and simulation studies. Soil Biology & Biochemistry 27, 1589–1599.
Soil pH and organic C dynamics in tropical forest soils: Evidence from laboratory and simulation studies.Crossref | GoogleScholarGoogle Scholar |

Naafs DFW, van Bergen PF, Boogert SJ, de Leeuw JW (2004) Solvent-extractable lipids in an acid andic forest soil; variations with depth and season. Soil Biology & Biochemistry 36, 297–308.
Solvent-extractable lipids in an acid andic forest soil; variations with depth and season.Crossref | GoogleScholarGoogle Scholar |

Neidleman SL (1987) Effects of temperature on lipid unsaturation. Biotechnology & Genetic Engineering Reviews 5, 245–268.
Effects of temperature on lipid unsaturation.Crossref | GoogleScholarGoogle Scholar |

Ohlrogge J, Browse J (1995) Lipid biosynthesis. The Plant Cell 7, 957–970.
Lipid biosynthesis.Crossref | GoogleScholarGoogle Scholar | 7640528PubMed |

Olsson PA, Wilhelmsson P (2000) The growth of external AM fungal mycelium in sand dunes and in experimental systems. Plant and Soil 226, 161–169.
The growth of external AM fungal mycelium in sand dunes and in experimental systems.Crossref | GoogleScholarGoogle Scholar |

Olsson PA, Bååth E, Jakobsen I, Söderström B (1995) The use of phospholipid and neutral lipid fatty-acids to estimate biomass of arbuscular mycorrhizal fungi in soil. Mycological Research 99, 623–629.
The use of phospholipid and neutral lipid fatty-acids to estimate biomass of arbuscular mycorrhizal fungi in soil.Crossref | GoogleScholarGoogle Scholar |

Olsson PA, Bååth E, Jakobsen I (1997) Phosphorus effects on the mycelium and storage structures of an arbuscular mycorrhizal fungus as studied in the soil and roots by analysis of fatty acid signatures. Applied and Environmental Microbiology 63, 3531–3538.
Phosphorus effects on the mycelium and storage structures of an arbuscular mycorrhizal fungus as studied in the soil and roots by analysis of fatty acid signatures.Crossref | GoogleScholarGoogle Scholar | 16535691PubMed |

Parmegiani RM, Pisano MA (1974) Effect of temperature on the triglyceride and phospholipid fatty acids of antibiotic-producing fungi. Developments in Industrial Microbiology 15, 318–323.

Peterse F, Hopmans EC, Schouten S, Mets A, Rijpstra WIC, Damste JSS (2011) Identification and distribution of intact polar branched tetraether lipids in peat and soil. Organic Geochemistry 42, 1007–1015.
Identification and distribution of intact polar branched tetraether lipids in peat and soil.Crossref | GoogleScholarGoogle Scholar |

Pollierer M, Scheu S, Haubert D (2010) Taking it to the next level: Trophic transfer of marker fatty acids from basal resource to predators. Soil Biology & Biochemistry 42, 919–925.
Taking it to the next level: Trophic transfer of marker fatty acids from basal resource to predators.Crossref | GoogleScholarGoogle Scholar |

Popko J, Herrfurth C, Feussner K, Ischebeck T, Iven T, Haslam R, Hamilton M, Sayanova O, Napier J, Khozin-Goldberg I, Feussner I (2016) Metabolome analysis reveals betaine lipids as major source for triglyceride formation, and the accumulation of sedoheptulose during nitrogen-starvation of Phaeodactylum tricornutum. PLoS One 11,
Metabolome analysis reveals betaine lipids as major source for triglyceride formation, and the accumulation of sedoheptulose during nitrogen-starvation of Phaeodactylum tricornutum.Crossref | GoogleScholarGoogle Scholar | 27736949PubMed |

Ratledge C (2008) Microbial Lipids. In ‘Biotechnology’. (Eds HJ Rehm, G Reed.) pp. 133–197. (VCH) https://doi.org/10.1002/9783527620999.ch4g

Riekhof WR, Naik S, Bertrand H, Benning C, Voelker DR (2014) Phosphate starvation in fungi induces the replacement of phosphatidylcholine with the phosphorus-free betaine lipid diacylglyceryl-N,N,N-trimethylhomoserine. Eukaryotic Cell 13, 749–757.
Phosphate starvation in fungi induces the replacement of phosphatidylcholine with the phosphorus-free betaine lipid diacylglyceryl-N,N,N-trimethylhomoserine.Crossref | GoogleScholarGoogle Scholar | 24728191PubMed |

Rinnan R, Bååth E (2009) Differential utilization of carbon substrates by bacteria and fungi in Tundra soil. Applied and Environmental Microbiology 75, 3611–3620.
Differential utilization of carbon substrates by bacteria and fungi in Tundra soil.Crossref | GoogleScholarGoogle Scholar | 19363072PubMed |

Roughan PG, Batt RD (1969) The glycerolipid composition of leaves. Phytochemistry 8, 363–369.
The glycerolipid composition of leaves.Crossref | GoogleScholarGoogle Scholar |

Rousk J, Brookes PC, Bååth E (2009) Contrasting Soil pH Effects on Fungal and Bacterial Growth Suggest Functional Redundancy in Carbon Mineralization. Applied and Environmental Microbiology 75, 1589–1596.
Contrasting Soil pH Effects on Fungal and Bacterial Growth Suggest Functional Redundancy in Carbon Mineralization.Crossref | GoogleScholarGoogle Scholar | 19151179PubMed |

Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. The ISME Journal 4, 1340–1351.
Soil bacterial and fungal communities across a pH gradient in an arable soil.Crossref | GoogleScholarGoogle Scholar | 20445636PubMed |

Schubotz F (2018) Membrane Homeostasis upon Nutrient (C, N, P) Limitation. In ‘Biogenesis of Fatty Acids, Lipids and Membranes’. (Ed. O Geiger.) pp. 1–25. (Springer International Publishing: Cham)

Sebastián M, Smith AF, Gonzalez JM, Fredricks HF, Van Mooy B, Koblizek M, Brandsma J, Koster G, Mestre M, Mostajir B, Pitta P, Postle AD, Sanchez P, Gasol JM, Scanlan DJ, Chen Y (2016) Lipid remodelling is a widespread strategy in marine heterotrophic bacteria upon phosphorus deficiency. The ISME Journal 10, 968–978.
Lipid remodelling is a widespread strategy in marine heterotrophic bacteria upon phosphorus deficiency.Crossref | GoogleScholarGoogle Scholar | 26565724PubMed |

Senesi N, Loffredo E (1999) The chemistry of soil organic matter. In ‘Soil Physical Chemistry. Second Edition’. (Ed. DL Sparks.) pp. 239–370. (CRC Press: USA)

Shimada H, Nemoto N, Shida Y, Oshima T, Yamagishi A (2008) Effects of pH and temperature on the composition of polar lipids in Thermoplasma acidophilum HO-62. Journal of Bacteriology 190, 5404–5411.
Effects of pH and temperature on the composition of polar lipids in Thermoplasma acidophilum HO-62.Crossref | GoogleScholarGoogle Scholar | 18539746PubMed |

Siles JA, Margesin R (2016) Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: what are the driving factors? Microbial Ecology 72, 207–220.
Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: what are the driving factors?Crossref | GoogleScholarGoogle Scholar | 26961712PubMed |

Siles JA, Cajthaml T, Minerbi S, Margesin R (2016) Effect of altitude and season on microbial activity, abundance and community structure in Alpine forest soils. FEMS Microbiology Ecology 92,
Effect of altitude and season on microbial activity, abundance and community structure in Alpine forest soils.Crossref | GoogleScholarGoogle Scholar | 26787774PubMed |

Siliakus MF, van der Oost J, Kengen SWM (2017) Adaptations of archaeal and bacterial membranes to variations in temperature, pH and pressure. Extremophiles 21, 651–670.
Adaptations of archaeal and bacterial membranes to variations in temperature, pH and pressure.Crossref | GoogleScholarGoogle Scholar | 28508135PubMed |

Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecology Letters 11, 1252–1264.
Stoichiometry of soil enzyme activity at global scale.Crossref | GoogleScholarGoogle Scholar | 18823393PubMed |

Skrupski B, Wilson KE, Goff KL, Zou J (2013) Effect of pH on neutral lipid and biomass accumulation in microalgal strains native to the Canadian prairies and the Athabasca oil sands. Journal of Applied Phycology 25, 937–949.
Effect of pH on neutral lipid and biomass accumulation in microalgal strains native to the Canadian prairies and the Athabasca oil sands.Crossref | GoogleScholarGoogle Scholar |

Sohlenkamp C, Geiger O (2016) Bacterial membrane lipids: diversity in structures and pathways. FEMS Microbiology Reviews 40, 133–159.
Bacterial membrane lipids: diversity in structures and pathways.Crossref | GoogleScholarGoogle Scholar | 25862689PubMed |

Sollich M, Yoshinaga MY, Häusler S, Price RE, Hinrichs K-U, Bühring SI (2017) Heat stress dictates microbial lipid composition along a thermal gradient in marine sediments. Frontiers in Microbiology 8, 1550
Heat stress dictates microbial lipid composition along a thermal gradient in marine sediments.Crossref | GoogleScholarGoogle Scholar | 28878741PubMed |

Stevenson FJ (1966) Lipids in soil. Journal of the American Oil Chemists’ Society 43, 203–210.
Lipids in soil.Crossref | GoogleScholarGoogle Scholar |

Strickland M, Rousk J (2010) Considering fungal: Bacterial dominance in soils – Methods, controls, and ecosystem implications. Soil Biology & Biochemistry 42, 1385–1395.
Considering fungal: Bacterial dominance in soils – Methods, controls, and ecosystem implications.Crossref | GoogleScholarGoogle Scholar |

Sundqvist MK, Liu ZF, Giesler R, Wardle DA (2014) Plant and microbial responses to nitrogen and phosphorus addition across an elevational gradient in subarctic tundra. Ecology 95, 1819–1835.
Plant and microbial responses to nitrogen and phosphorus addition across an elevational gradient in subarctic tundra.Crossref | GoogleScholarGoogle Scholar | 25163116PubMed |

Taguchi Y-h, Oono Y (2005) Relational patterns of gene expression via non-metric multidimensional scaling analysis. Bioinformatics 21, 730–740.
Relational patterns of gene expression via non-metric multidimensional scaling analysis.Crossref | GoogleScholarGoogle Scholar | 15509613PubMed |

van Bergen PF, Bull ID, Poulton PR, Evershed RP (1997) Organic geochemical studies of soils from the Rothamsted Classical Experiments—I. Total lipid extracts, solvent insoluble residues and humic acids from Broadbalk Wilderness. Organic Geochemistry 26, 117–135.
Organic geochemical studies of soils from the Rothamsted Classical Experiments—I. Total lipid extracts, solvent insoluble residues and humic acids from Broadbalk Wilderness.Crossref | GoogleScholarGoogle Scholar |

Van Mooy BAS, Fredricks HF, Pedler BE, Dyhrman ST, Karl DM, Koblizek M, Lomas MW, Mincer TJ, Moore LR, Moutin T, Rappe MS, Webb EA (2009) Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature 458, 69–72.
Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity.Crossref | GoogleScholarGoogle Scholar |

Vokt JP, Brody S (1985) The kinetics of changes in the fatty acid composition of Neurospora crassa lipids after a temperature increase. Biochimica et Biophysica Acta 835, 176–182.
The kinetics of changes in the fatty acid composition of Neurospora crassa lipids after a temperature increase.Crossref | GoogleScholarGoogle Scholar | 3159434PubMed |

Warren CR (2017) Variation in small organic N compounds and amino acid enantiomers along an altitudinal gradient. Soil Biology & Biochemistry 115, 197–212.
Variation in small organic N compounds and amino acid enantiomers along an altitudinal gradient.Crossref | GoogleScholarGoogle Scholar |

Warren CR (2018) A liquid chromatography-mass spectrometry method for analysis of intact fatty-acid-based lipids extracted from soil. European Journal of Soil Science 69, 791–803.
A liquid chromatography-mass spectrometry method for analysis of intact fatty-acid-based lipids extracted from soil.Crossref | GoogleScholarGoogle Scholar |

Warren CR (2019) Does silica solid-phase extraction of soil lipids isolate a pure phospholipid fraction. Soil Biology & Biochemistry 128, 175–178.
Does silica solid-phase extraction of soil lipids isolate a pure phospholipid fraction.Crossref | GoogleScholarGoogle Scholar |

Warren CR (2020) Soil microbial populations substitute phospholipids with betaine lipids in response to low P availability. Soil Biology & Biochemistry 140, 107655
Soil microbial populations substitute phospholipids with betaine lipids in response to low P availability.Crossref | GoogleScholarGoogle Scholar |

White DC (1993) In situ measurement of microbial biomass, community structure and nutritional status. Philosophical Transactions of the Royal Society of London Series a-Mathematical Physical and Engineering Sciences 344, 59–67.
In situ measurement of microbial biomass, community structure and nutritional status.Crossref | GoogleScholarGoogle Scholar |

Wintermans JFGM (1960) Concentrations of phosphatides and glycolipids in leaves and chloroplasts. Biochimica et Biophysica Acta 44, 49–54.
Concentrations of phosphatides and glycolipids in leaves and chloroplasts.Crossref | GoogleScholarGoogle Scholar |

Wood TG (1970) Decomposition of Plant Litter in Montane and Alpine Soils on Mt-Kosciusko, Australia. Nature 226, 561
Decomposition of Plant Litter in Montane and Alpine Soils on Mt-Kosciusko, Australia.Crossref | GoogleScholarGoogle Scholar | 16057384PubMed |

Wörmer L, Lipp JS, Hinrichs K-U (2017) Comprehensive analysis of microbial lipids in environmental samples through HPLC-MS protocols. In ‘Hydrocarbon and lipid microbiology protocols: petroleum, hydrocarbon and lipid Analysis’. (Eds TJ McGenity, KN Timmis, B Nogales.) pp. 289–317. (Springer: Berlin)

Wu J, Anderson BJ, Buckley HL, Lewis G, Lear G (2017) Aspect has a greater impact on alpine soil bacterial community structure than elevation. FEMS Microbiology Ecology 93, fiw253
Aspect has a greater impact on alpine soil bacterial community structure than elevation.Crossref | GoogleScholarGoogle Scholar | 29126231PubMed |

Zelles L (1997) Phospholipid fatty acid profiles in selected members of soil microbial communities. Chemosphere 35, 275–294.
Phospholipid fatty acid profiles in selected members of soil microbial communities.Crossref | GoogleScholarGoogle Scholar | 9232001PubMed |

Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biology and Fertility of Soils 29, 111–129.
Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review.Crossref | GoogleScholarGoogle Scholar |

Zhang B, Liang C, He HB, Zhang XD (2013) Variations in soil microbial communities and residues along an altitude gradient on the northern slope of Changbai Mountain, China. PLoS One 8,
Variations in soil microbial communities and residues along an altitude gradient on the northern slope of Changbai Mountain, China.Crossref | GoogleScholarGoogle Scholar | 24386147PubMed |

Zhang H, Zeng R, Chen D, Liu J (2016) A pivotal role of vacuolar H+-ATPase in regulation of lipid production in Phaeodactylum tricornutum. Scientific Reports 6, 31319
A pivotal role of vacuolar H+-ATPase in regulation of lipid production in Phaeodactylum tricornutum.Crossref | GoogleScholarGoogle Scholar | 27499168PubMed |

Zhang Y, Zheng N, Wang J, Yao H, Qiu Q, Chapman SJ (2019) High turnover rate of free phospholipids in soil confirms the classic hypothesis of PLFA methodology. Soil Biology & Biochemistry 135, 323–330.
High turnover rate of free phospholipids in soil confirms the classic hypothesis of PLFA methodology.Crossref | GoogleScholarGoogle Scholar |

Ziegler F, Zech W (1989) Distribution pattern of total lipids and lipid fractions in forest humus. Zeitschrift für Pflanzenernährung und Bodenkunde 152, 287–290.
Distribution pattern of total lipids and lipid fractions in forest humus.Crossref | GoogleScholarGoogle Scholar |