Microbial carbon use efficiency: accounting for population, community, and ecosystem-scale controls over the fate of metabolized organic matter

Biogeochemistry

Volumn 127, Issue 2-3, 2016, Pages 173-188

  Geyer, Kevin M ^a   Kyker Snowman, Emily ^a   Grandy, A Stuart ^a   Frey, Serita D ^a  

^a UNIVERSITY OF NEW HAMPSHIRE   (United States)

Author keywords

Carbon cycling; Carbon use efficiency; Microbial ecology; Microbial metabolism

Indexed keywords

BIOGEOCHEMISTRY; BIOMASS; CARBON FLUX; CARBON SEQUESTRATION; COMMUNITY DYNAMICS; GROWTH RATE; METABOLISM; MICROBIAL ACTIVITY; MICROBIAL ECOLOGY; POPULATION DYNAMICS; SOIL MICROORGANISM; SOIL ORGANIC MATTER; SPATIOTEMPORAL ANALYSIS; TERRESTRIAL ENVIRONMENT; THERMODYNAMICS;

EID: 84959476104     PISSN: 01682563     EISSN: 1573515X     Source Type: Journal    
DOI: 10.1007/s10533-016-0191-y     Document Type: Article

References (88)

1. Alden L, Demoling F, Baath E (2001) Rapid method of determining factors limiting bacterial growth in soil. Appl Environ Microbiol 67:1830–1838
2. Allison SD (2014) Modeling adaptation of carbon use efficiency in microbial communities. Front Microbiol 5:9
3. Amado AM, Meirelles-Pereira F, Vidal LO, Sarmento H, Suhett AL, Farjalla VF, Cotner JB, Roland F (2013) Tropical freshwater ecosystems have lower bacterial growth efficiency than temperate ones. Front Microbiol 4:8
4. Angulo-Brown F, Santillan M, Callejaquevedo E (1995) Thermodynamic optimality in some biochemical reactions. Nuovo Cimento Soc Ital Fis D-Condens Matter At Mol Chem Phys Fluids Plasmas Biophys 17:87–90
5. Apple JK, del Giorgio P (2007) Organic substrate quality as the link between bacterioplankton carbon demand and growth efficiency in a temperate salt-marsh estuary. ISME J 1:729–742
6. Apple JK, del Giorgi PA, Kemp WM (2006) Temperature regulation of bacterial production, respiration, and growth efficiency in a temperate salt-marsh estuary. Aquat Microb Ecol 43:243–254
7. Babel W (2009) The Auxiliary Substrate Concept: from simple considerations to heuristically valuable knowledge. Eng Life Sci 9:285–290
8. Barros N, Salgado J, Rodriguez-Anon JA, Proupin J, Villanueva M, Hansen LD (2010) Calorimetric approach to metabolic carbon conversion efficiency in soils. J Therm Anal Calorim 99:771–777
9. Blagodatskaya E, Blagodatsky S, Anderson TH, Kuzyakov Y (2014) Microbial growth and carbon use efficiency in the rhizosphere and root-free soil. PLoS One 9:9
10. Blazewicz SJ, Schwartz E (2011) Dynamics of O-18 incorporation from H (2) (18) O into soil microbial DNA. Microb Ecol 61:911–916
11. Bol R, Poirier N, Balesdent J, Gleixner G (2009) Molecular turnover time of soil organic matter in particle-size fractions of an arable soil. Rapid Commun Mass Spectrom 23:2551–2558
12. Bott T (2006) Primary productivity and community respiration. In: Hauer FR, Lamberti GA (eds) Methods in stream ecology. Academic Press, Cambridge, pp 663–690
13. Brant JB, Sulzman EW, Myrold DD (2006) Microbial community utilization of added carbon substrates in response to long-term carbon input manipulation. Soil Biol Biochem 38:2219–2232
14. Bremer E, Kuikman P (1994) Microbial utilization of C-14 U glucose in soil is affected by the amount and timing of glucose additions. Soil Biol Biochem 26:511–517
15. Cole JJ, Findlay S, Pace ML (1988) Bacterial production in fresh and saltwater ecosystems—a cross-system overview. Mar Ecol Prog Ser 43:1–10
16. Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E (2013) The microbial efficiency-matrix stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob Change Biol 19:988–995
17. Creamer CA, Jones DL, Baldock JA, Farrell M (2014) Stoichiometric controls upon low molecular weight carbon decomposition. Soil Biol Biochem 79:50–56
18. Dawes EA, Ribbons DW (1964) Some aspects of endogenous metabolism of bacteria. Bacteriol Rev 28:126
19. del Giorgio PA, Cole JJ (1998) Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Syst 29:503–541
20. del Giorgio PA, Newell REI (2012) Phosphorus and DOC availability influence the partitioning between bacterioplankton production and respiration in tidal marsh ecosystems. Environ Microbiol 14:1296–1307
21. Devevre OC, Horwath WR (2000) Decomposition of rice straw and microbial carbon use efficiency under different soil temperatures and moistures. Soil Biol Biochem 32:1773–1785
22. Dijkstra P, Blankinship JC, Selmants PC, Hart SC, Koch GW, Schwartz E, Hungate BA (2011a) Probing carbon flux patterns through soil microbial metabolic networks using parallel position-specific tracer labeling. Soil Biol Biochem 43:126–132
23. Dijkstra P, Dalder JJ, Selmants PC, Hart SC, Koch GW, Schwartz E, Hungate BA (2011b) Modeling soil metabolic processes using isotopologue pairs of position-specific C-13-labeled glucose and pyruvate. Soil Biol Biochem 43:1848–1857
24. Dijkstra P, Thomas SC, Heinrich PL, Koch GW, Schwartz E, Hungate BA (2011c) Effect of temperature on metabolic activity of intact microbial communities: evidence for altered metabolic pathway activity but not for increased maintenance respiration and reduced carbon use efficiency. Soil Biol Biochem 43:2023–2031
25. Elliott ET, Cole CV, Fairbanks BC, Woods LE, Bryant RJ, Coleman DC (1983) Short-term bacterial growth, nutrient uptake, and ATP turnover in sterilized, inoculated and C-amended soil—the influence of N availability. Soil Biol Biochem 15:85–91
26. Fonte ES, Amado AM, Meirelles-Pereira F, Esteves FA, Rosado AS, Farjalla VF (2013) The combination of different carbon sources enhances bacterial growth efficiency in aquatic ecosystems. Microb Ecol 66:871–878
27. Frey SD, Gupta V, Elliott ET, Paustian K (2001) Protozoan grazing affects estimates of carbon utilization efficiency of the soil microbial community. Soil Biol Biochem 33:1759–1768
28. Frey S, Lee J, Melillo JM, Six J (2013) The temperature response of soil microbial efficiency and its feedback to climate. Nat Clim Change 3:395–398
29. Fuhrman JA, Azam F (1980) Bacterioplankton secondary production estimates for coastal waters of British-Colombia, Antarctica, and California. Appl Environ Microbiol 39:1085–1095
30. Gommers PJF, Vanschie BJ, Vandijken JP, Kuenen JG (1988) Biochemical limits to microbial growth yields—an analysis of mixed substrate utilization. Biotechnol Bioeng 32:86–94
31. Grandy AS, Strickland MS, Lauber CL, Bradford MA, Fierer N (2009) The influence of microbial communities, management, and soil texture on soil organic matter chemistry. Geoderma 150:278–286
32. Hagerty S, van Groenigen KJ, Allison SD, Hungate BA, Schwartz E, Koch GW, Kolka RK, Dijkstra P (2014) Accelerated microbial turnover but constant growth efficiency with warming in soil. Nat Clim Change 4:903–906
33. Harris JA, Ritz K, Coucheney E, Grice SM, Lerch TZ, Pawlett M, Herrmann AM (2012) The thermodynamic efficiency of soil microbial communities subject to long-term stress is lower than those under conventional input regimes. Soil Biol Biochem 47:149–157
34. Herrmann AM, Coucheney E, Nunan N (2014) Isothermal microcalorimetry provides new insight into terrestrial carbon cycling. Environ Sci Technol 48:4344–4352
35. Hill PW, Farrar JF, Jones DL (2008) Decoupling of microbial glucose uptake and mineralization in soil. Soil Biol Biochem 40:616–624
36. Hunt HW, Cole CV, Elliott ET (1985) Models for growth of bacteria inoculated into sterilized soil. Soil Sci 139:156–165
37. Ingraham JL, Maaloe O, Neidhardt FC (1983) Growth of the bacterial cell. Sinauer Associates Inc, Sunderland
38. Jenkinson DS (1968) Turnover of organic matter in soil. Biochem J 109:P2
39. Karhu K, Auffret MD, Dungait JAJ, Hopkins DW, Prosser JI, Singh BK, Subke JA, Wookey PA, Agren GI, Sebastia MT, Gouriveau F, Bergkvist G, Meir P, Nottingham AT, Salinas N, Hartley IP (2014) Temperature sensitivity of soil respiration rates enhanced by microbial community response. Nature 513:81
40. Kawasaki N, Benner R (2006) Bacterial release of dissolved organic matter during cell growth and decline: molecular origin and composition. Limnol Oceanogr 51:2170–2180
41. Keiblinger KM, Hall EK, Wanek W, Szukics U, Hammerle I, Ellersdorfer G, Bock S, Strauss J, Sterflinger K, Richter A, Zechmeister-Boltenstern S (2010) The effect of resource quantity and resource stoichiometry on microbial carbon-use-efficiency. FEMS Microbiol Ecol 73:430–440
42. Kim B, Gadd G (2008) Bacterial physiology and metabolism. Cambridge University Press, New York
43. Kosolapov DB, Kosolapova NG, Rumyantseva EV (2014) Activity and growth efficiency of heterotrophic bacteria in Rybinsk Reservoir. Biol Bull 41:324–332
44. Kredics L, Antal Z, Manczinger L (2000) Influence of water potential on growth, enzyme secretion and in vitro enzyme activities of Trichoderma harzianum at different temperatures. Curr Microbiol 40:310–314
45. Lee ZM, Schmidt TM (2014) Bacterial growth efficiency varies in soils under different land management practices. Soil Biol Biochem 69:282–290
46. Lemee R, Rochelle-Newall E, Van Wambeke F, Pizay MD, Rinaldi P, Gattuso JP (2002) Seasonal variation of bacterial production, respiration and growth efficiency in the open NW Mediterranean Sea. Aquat Microb Ecol 29:227–237
47. Lindeman RL (1942) The trophic-dynamic aspect of ecology. Ecology 23:399–418
48. Linton JD, Stephenson RJ (1978) A preliminary study on growth yields in relation to carbon and energy content of various organic growth substrates. FEMS Microbiol Lett 3:95–98
49. Lipson DA, Monson RK, Schmidt SK, Weintraub MN (2009) The trade-off between growth rate and yield in microbial communities and the consequences for under-snow soil respiration in a high elevation coniferous forest. Biogeochemistry 95:23–35
50. Manzoni S, Jackson RB, Trofymow JA, Porporato A (2008) The global stoichiometry of litter nitrogen mineralization. Science 321:684–686
51. Manzoni S, Taylor P, Richter A, Porporato A, Agren GI (2012) Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol 196:79–91
52. Marr AG, Nilson EH, Clark DJ (1963) The maintenance requirement of Escherichia coli. Ann N Y Acad Sci 102:548
53. Moorhead DL, Lashermes G, Sinsabaugh RL (2012) A theoretical model of C- and N-acquiring exoenzyme activities, which balances microbial demands during decomposition. Soil Biol Biochem 53:133–141
54. Mooshammer M, Wanek W, Zechmeister-Boltenstern S, Richter A (2014) Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources. Front Microbiol 5:10
55. Neidhardt FC, Ingraham JL, Schaechter M (1990) Physiology of the bacterial cell: a molecular approach. Sinauer Associates Inc, Sunderland
56. Nguyen C, Guckert A (2001) Short-term utilisation of C-14 U glucose by soil microorganisms in relation to carbon availability. Soil Biol Biochem 33:53–60
57. Ortega-Retuerta E, Jeffrey WH, Babin M, Belanger S, Benner R, Marie D, Matsuoka A, Raimbault P, Joux F (2012) Carbon fluxes in the Canadian Arctic: patterns and drivers of bacterial abundance, production and respiration on the Beaufort Sea margin. Biogeosciences 9:3679–3692
58. Parton WJ, Schimel DS, Cole CV, Ojima DS (1987) Analysis of factors controlling soil organic matter levels in Great Plains grasslands USA. Soil Sci Soc Am J 51:1173–1179
59. Paustian K, Robertson GP, Elliott ET (1995) Management impacts on carbon storage and gas fluxes (C02, CH4) in mid-latitude cropland. In: Lal R, Kimble JM, Levine E, Stewart BA (eds) Soil management and the greenhouse effect. CRC Press, Boca Raton, pp 69–84
60. Payne WJ, Wiebe WJ (1978) Growth yield and efficiency in chemosynthetic microorganisms. Annu Rev Microbiol 32:155–183
61. Pfeiffer T, Schuster S, Bonhoeffer S (2001) Cooperation and competition in the evolution of ATP-producing pathways. Science 292:504–507
62. Pirt SJ (1965) The maintenance energy of bacteria in growing cultures. Proc R Soc Lond Ser B-Biol Sci 163:224–231
63. Ram ASP, Nair S, Chandramohan D (2003) Bacterial growth efficiency in the tropical estuarine and coastal waters of Goa, southwest coast of India. Microb Ecol 45:88–96
64. Reischke S, Rousk J, Baath E (2014) The effects of glucose loading rates on bacterial and fungal growth in soil. Soil Biol Biochem 70:88–95
65. Rivkin RB, Legendre L (2001) Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Science 291:2398–2400
66. Roels JA (1980) Application of macroscopic principles to microbial metabolism. Biotechnol Bioeng 22:2457–2514
67. Roller BRK, Schmidt TM (2015) The physiology and ecological implications of efficient growth. Int Soc Microb Ecol 9:1481–1487. doi:10.1038/ismej.2014.235
68. Rousk J, Baath E (2007) Fungal and bacterial growth in soil with plant materials of different C/N ratios. FEMS Microbiol Ecol 62:258–267
69. Rousk J, Baath E (2011) Growth of saprotrophic fungi and bacteria in soil. FEMS Microbiol Ecol 78:17–30
70. Russell JB, Cook GM (1995) Energetics of bacterial growth—balance of anabolic and catabolic reactions. Microbiol Rev 59:48–62
71. Schipper LA, Hobbs JK, Rutledge S, Arcus VL (2014) Thermodynamic theory explains the temperature optima of soil microbial processes and high Q(10) values at low temperatures. Glob Change Biol 20:3578–3586
72. Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Koegel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature (London) 478:49–56
73. Sinsabaugh RL, Manzoni S, Moorhead DL, Richter A (2013) Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecol Lett 16:930–939
74. Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–569
75. Sorensen LH (1987) Organic-matter and microbial biomass in a soil incubated in the field for 20 years with C-14-labeled barley straw. Soil Biol Biochem 19:39–42
76. Tang YJ, Martin HG, Myers S, Rodriguez S, Baidoo EEK, Keasling JD (2009) Advances in analysis of microbial metabolic fluxes via C-13 isotopic labeling. Mass Spectrom Rev 28:362–375
77. Tang JKH, You L, Blankenship RE, Tang YJJ (2012) Recent advances in mapping environmental microbial metabolisms through C-13 isotopic fingerprints. J R Soc Interface 9:2767–2780
78. Tannler S, Decasper S, Sauer U (2008) Maintenance metabolism and carbon fluxes in Bacillus species. Microb Cell Fact 7:13
79. Thiet RK, Frey SD, Six J (2006) Do growth yield efficiencies differ between soil microbial communities differing in fungal: bacterial ratios? Reality check and methodological issues. Soil Biol Biochem 38:837–844
80. Tiemann LK, Billings SA (2011) Changes in variability of soil moisture alter microbial community C and N resource use. Soil Biol Biochem 43:1837–1847
81. Vallino JJ, Hopkinson CS, Hobbie JE (1996) Modeling bacterial utilization of dissolved organic matter: optimization replaces monod growth kinetics. Limnol Oceanogr 41:1591–1609
82. von Stockar U, Maskow T, Liu JS, Marison IW, Patino R (2006) Thermodynamics of microbial growth and metabolism: an analysis of the current situation. J Biotechnol 121:517–533
83. Voroney RP, Paul EA, Anderson DW (1989) Decomposition of wheat straw and stabilization of microbial products. Can J Soil Sci 69:63–77
84. Wang GS, Post WM (2012) A theoretical reassessment of microbial maintenance and implications for microbial ecology modeling. FEMS Microbiol Ecol 81:610–617
85. Wang GS, Post WM, Mayes MA (2013) Development of microbial-enzyme-mediated decomposition model parameters through steady-state and dynamic analyses. Ecol Appl 23:255–272
86. Ward A (2006) Heterotrophic bacteria. In: Hauer FR, Lamberti GA (eds) Methods in stream ecology. Academic Press, Cambridge, pp 293–309
87. Wieder WR, Grandy AS, Kallenbach CM, Bonan GB (2014) Integrating microbial physiology and physio-chemical principles in soils with the microbial-mineral carbon stabilization (MIMICS) model. Biogeosciences 11:3899–3917
88. Zhang YHP, Lynd LR (2005) Cellulose utilization by Clostridium thermocellum: bioenergetics and hydrolysis product assimilation. Proc Natl Acad Sci USA 102:7321–7325