Experimental demonstration of chaotic instability in biological nitrification

David W. Graham, Charles W. Knapp, Erik S. Van Vleck, Katie Bloor, Teresa B. Lane, Christopher E. Graham

Research output: Contribution to journalArticle

180 Citations (Scopus)

Abstract

Biological nitrification (that is, NH3 -> NO2- -> NO3-) is a key reaction in the global nitrogen cycle (N-cycle); however, it is also known anecdotally to be unpredictable and sometimes fails inexplicably. Understanding the basis of unpredictability in nitrification is critical because the loss or impairment of this function might influence the balance of nitrogen in the environment and also has biotechnological implications. One explanation for unpredictability is the presence of chaotic behavior; however, proving such behavior from experimental data is not trivial, especially in a complex microbial community. Here, we show that chaotic behavior is central to stability in nitrification because of a fragile mutualistic relationship between ammonia-oxidizing bacteria (AOB) and nitrite-oxidizing bacteria (NOB), the two major guilds in nitrification. Three parallel chemostats containing mixed microbial communities were fed complex media for 207 days, and nitrification performance, and abundances of AOB, NOB, total bacteria and protozoa were quantified over time. Lyapunov exponent calculations, supported by surrogate data and other tests, showed that all guilds were sensitive to initial conditions, suggesting broad chaotic behavior. However, NOB were most unstable among guilds and displayed a different general pattern of instability. Further, NOB variability was maximized when AOB were most unstable, which resulted in erratic nitrification including significant NO2- accumulation. We conclude that nitrification is prone to chaotic behavior because of a fragile AOB-NOB mutualism, which must be considered in all systems that depend on this critical reaction.
Original languageEnglish
Pages (from-to)385-393
Number of pages8
JournalISME Journal
Volume1
Issue number5
DOIs
Publication statusPublished - Sep 2007

Fingerprint

Nitrification
nitrification
Bacteria
bacterium
bacteria
Nitrites
nitrites
nitrite
ammonia
Ammonia
guild
microbial communities
microbial community
Nitrogen Cycle
chemostat
nitrogen cycle
Symbiosis
mutualism
erratic
nitrogen balance

Keywords

  • chaotic behavior
  • lyapunov exponents
  • nitrification
  • mutualism
  • N-cycle

Cite this

Graham, D. W., Knapp, C. W., Van Vleck, E. S., Bloor, K., Lane, T. B., & Graham, C. E. (2007). Experimental demonstration of chaotic instability in biological nitrification. ISME Journal, 1(5), 385-393. https://doi.org/10.1038/ismej.2007.45
Graham, David W. ; Knapp, Charles W. ; Van Vleck, Erik S. ; Bloor, Katie ; Lane, Teresa B. ; Graham, Christopher E. / Experimental demonstration of chaotic instability in biological nitrification. In: ISME Journal. 2007 ; Vol. 1, No. 5. pp. 385-393.
@article{8a33172dc9d6462c8b71b53a63541f2e,
title = "Experimental demonstration of chaotic instability in biological nitrification",
abstract = "Biological nitrification (that is, NH3 -> NO2- -> NO3-) is a key reaction in the global nitrogen cycle (N-cycle); however, it is also known anecdotally to be unpredictable and sometimes fails inexplicably. Understanding the basis of unpredictability in nitrification is critical because the loss or impairment of this function might influence the balance of nitrogen in the environment and also has biotechnological implications. One explanation for unpredictability is the presence of chaotic behavior; however, proving such behavior from experimental data is not trivial, especially in a complex microbial community. Here, we show that chaotic behavior is central to stability in nitrification because of a fragile mutualistic relationship between ammonia-oxidizing bacteria (AOB) and nitrite-oxidizing bacteria (NOB), the two major guilds in nitrification. Three parallel chemostats containing mixed microbial communities were fed complex media for 207 days, and nitrification performance, and abundances of AOB, NOB, total bacteria and protozoa were quantified over time. Lyapunov exponent calculations, supported by surrogate data and other tests, showed that all guilds were sensitive to initial conditions, suggesting broad chaotic behavior. However, NOB were most unstable among guilds and displayed a different general pattern of instability. Further, NOB variability was maximized when AOB were most unstable, which resulted in erratic nitrification including significant NO2- accumulation. We conclude that nitrification is prone to chaotic behavior because of a fragile AOB-NOB mutualism, which must be considered in all systems that depend on this critical reaction.",
keywords = "chaotic behavior, lyapunov exponents, nitrification, mutualism, N-cycle",
author = "Graham, {David W.} and Knapp, {Charles W.} and {Van Vleck}, {Erik S.} and Katie Bloor and Lane, {Teresa B.} and Graham, {Christopher E.}",
year = "2007",
month = "9",
doi = "10.1038/ismej.2007.45",
language = "English",
volume = "1",
pages = "385--393",
journal = "ISME Journal",
issn = "1751-7362",
number = "5",

}

Graham, DW, Knapp, CW, Van Vleck, ES, Bloor, K, Lane, TB & Graham, CE 2007, 'Experimental demonstration of chaotic instability in biological nitrification', ISME Journal, vol. 1, no. 5, pp. 385-393. https://doi.org/10.1038/ismej.2007.45

Experimental demonstration of chaotic instability in biological nitrification. / Graham, David W.; Knapp, Charles W.; Van Vleck, Erik S.; Bloor, Katie; Lane, Teresa B.; Graham, Christopher E.

In: ISME Journal, Vol. 1, No. 5, 09.2007, p. 385-393.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Experimental demonstration of chaotic instability in biological nitrification

AU - Graham, David W.

AU - Knapp, Charles W.

AU - Van Vleck, Erik S.

AU - Bloor, Katie

AU - Lane, Teresa B.

AU - Graham, Christopher E.

PY - 2007/9

Y1 - 2007/9

N2 - Biological nitrification (that is, NH3 -> NO2- -> NO3-) is a key reaction in the global nitrogen cycle (N-cycle); however, it is also known anecdotally to be unpredictable and sometimes fails inexplicably. Understanding the basis of unpredictability in nitrification is critical because the loss or impairment of this function might influence the balance of nitrogen in the environment and also has biotechnological implications. One explanation for unpredictability is the presence of chaotic behavior; however, proving such behavior from experimental data is not trivial, especially in a complex microbial community. Here, we show that chaotic behavior is central to stability in nitrification because of a fragile mutualistic relationship between ammonia-oxidizing bacteria (AOB) and nitrite-oxidizing bacteria (NOB), the two major guilds in nitrification. Three parallel chemostats containing mixed microbial communities were fed complex media for 207 days, and nitrification performance, and abundances of AOB, NOB, total bacteria and protozoa were quantified over time. Lyapunov exponent calculations, supported by surrogate data and other tests, showed that all guilds were sensitive to initial conditions, suggesting broad chaotic behavior. However, NOB were most unstable among guilds and displayed a different general pattern of instability. Further, NOB variability was maximized when AOB were most unstable, which resulted in erratic nitrification including significant NO2- accumulation. We conclude that nitrification is prone to chaotic behavior because of a fragile AOB-NOB mutualism, which must be considered in all systems that depend on this critical reaction.

AB - Biological nitrification (that is, NH3 -> NO2- -> NO3-) is a key reaction in the global nitrogen cycle (N-cycle); however, it is also known anecdotally to be unpredictable and sometimes fails inexplicably. Understanding the basis of unpredictability in nitrification is critical because the loss or impairment of this function might influence the balance of nitrogen in the environment and also has biotechnological implications. One explanation for unpredictability is the presence of chaotic behavior; however, proving such behavior from experimental data is not trivial, especially in a complex microbial community. Here, we show that chaotic behavior is central to stability in nitrification because of a fragile mutualistic relationship between ammonia-oxidizing bacteria (AOB) and nitrite-oxidizing bacteria (NOB), the two major guilds in nitrification. Three parallel chemostats containing mixed microbial communities were fed complex media for 207 days, and nitrification performance, and abundances of AOB, NOB, total bacteria and protozoa were quantified over time. Lyapunov exponent calculations, supported by surrogate data and other tests, showed that all guilds were sensitive to initial conditions, suggesting broad chaotic behavior. However, NOB were most unstable among guilds and displayed a different general pattern of instability. Further, NOB variability was maximized when AOB were most unstable, which resulted in erratic nitrification including significant NO2- accumulation. We conclude that nitrification is prone to chaotic behavior because of a fragile AOB-NOB mutualism, which must be considered in all systems that depend on this critical reaction.

KW - chaotic behavior

KW - lyapunov exponents

KW - nitrification

KW - mutualism

KW - N-cycle

UR - http://www.nature.com/ismej/index.html

UR - http://dx.doi.org/10.1038/ismej.2007.45

U2 - 10.1038/ismej.2007.45

DO - 10.1038/ismej.2007.45

M3 - Article

VL - 1

SP - 385

EP - 393

JO - ISME Journal

JF - ISME Journal

SN - 1751-7362

IS - 5

ER -