Trimethylamine oxide accumulation as a function of depth in Hawaiian mid-water fishes

Abstract

6Trimethylamine oxide (TMAO) is a common osmolyte and counteracting solute. It is believed to 7 combat the denaturation induced by hydrostatic pressure as some deep-sea animals contain 8 higher TMAO levels than their shallow water counterparts. It has also been proposed that TMAO 9 may accumulate passively during lipid storage resulting in a correlation between lipid content 10 and TMAO levels in some groups. Previous research showed that lipid content decreased with 11 depth in species of Hawaiian fishes presenting a novel test of these competing hypotheses. 12 TMAO ranged from 20.4 to 92.8 mmol/kg. Lipid content ranged from 0.50 to 4.7 % WW. After 13 completing a comprehensive search for depths available in the literature, provided here, we 14 analyzed TMAO and lipid as a function of average, minimum and maximum depth of occurrence 15 for 27 species of fishes from nine orders. We found that TMAO is positively correlated with all 16 measures of habitat depth (hydrostatic pressure) but the relationship is strongest with average 17 depth. We further showed using phylogenetic independent contrasts that this relationship was not 18 influenced by the evolutionary relatedness of these species. Interestingly, we found that lipid 19 content increased with depth, in direct contrast to previous studies. TMAO is thus also 20 positively correlated with lipid content. While we are unable to distinguish between these 21 hypotheses, we show that TMAO is strongly correlated with depth in mid-water fishes. 22Key Words: trimethylamine oxide (TMAO); lipid; chemical composition; hydrostatic 23 pressure; depth; Hawaiian fish 24 335 20 We thank Jeff Drazen for his assistance identifying fishes. We also thank Bruce Mundy and the 336 Pacific Islands Fisheries Science Center, National Oceanic and Atmospheric Administration for 337 the invaluable references provided for identification of these fishes and constructive comments 338 on the manuscript. Additionally, we would like to thank the captain and crew of the R/V Kilo 339Moana and A. M. Sweeney for providing ship time.

Development and sexual dimorphism of the sonic system in three deep-sea neobythitine fishes and comparisons between upper mid and lower continental slope

“…This study compares the morphology and development of the sonic system of six neobythitine cusk-eels from depths of two to three hundred to five thousand meters. In addition to phylogentic changes (discussed later) there are potential twin effects on morphology from decreasing food supplies with depth (Lampitt et al, 1986;Collins et al, 2005;Sutton et al, 2010;Mindel et al, 2016) and increasing hydrostatic pressure (Angel, 1997;Bochus and Seibel, 2016). To our knowledge the effect of neither has been examined in terms of sonic morphology, a proxy for sound production since fish sounds have not been recorded from great depths (Fine and Parmentier, 2015).…”

“…In this paper we describe and quantify the sonic system of three Atlantic neobythitine species captured at respectively around 1 km and deeper (Dicrolene intronigra) and 1.6-5 km depths (Porogadus miles and Bathyonus pectoralis) for comparison with the upper slope Taiwanese species. The deeper two species live in an environment with great hydrostatic pressures (Angel, 1997;Bochus and Seibel, 2016) and little food (Lampitt et al, 1986;Collins et al, 2005;Sutton et al, 2010;Mindel et al, 2016). Owing to the food scarcity, we hypothesized that the sonic system would be reduced in deeper species.…”

Thermal Range and Physiological Tolerance Mechanisms in Two Shark Species from the Northwest Atlantic

“…Notably, accumulation of a small intracellular methylamine, trimethylamine N-oxide (TMAO), has been proposed as an alternative cytoprotective response to HSP70. TMAO has the ability to stabilize protein structure and conserve function (Yancey and Somero, 1979;Yancey and Siebenaller, 1999;Yancey et al, 2001) in response to a variety of destabilizing factors, including urea (Treberg et al, 2006), salinity (Pillans et al, 2005;Deck et al, 2016), hydrostatic pressure (Yancey et al, 2014;Bockus and Seibel, 2016), and temperature (see Seibel and Walsh, 2002;Yancey, 2005 for reviews). The majority of studies examining changes in TMAO content with thermal fluctuations have focused on teleost fishes and their response to cold acclimation.…”

How Osmolytes Counteract Pressure Denaturation on a Molecular Scale

“…[18–20] One of the osmolytes used by fish is trimethylamine N-oxide (TMAO), whose cellular concentration reportedly increases with sea depth, further highlighting their crucial role for survival in high pressure environments. [21] …”

“…[18][19][20] One of the osmolytes used by fish is trimethylamine N-oxide (TMAO), the cellular concentrationo f which reportedlyi ncreasesw ith sea depth, furtherh ighlighting the crucial role of osmolytes for survival in high pressure environments. [21] Mounting evidence suggests that osmolytes do indeed increase the stabilityo fn ative protein structures. [22][23][24][25][26] The native structure is generally more compact with as ignificantly smaller surfacea rea than the denatured state, as obtained by thermal and co-solvent-induced denaturation.…”