Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon

Abstract

An ammonia-oxidizing, carbon-fixing archaeon, Candidatus ''Nitrosopumilus maritimus,'' recently was isolated from a salt-water aquarium, definitively confirming that chemoautotrophy exists among the marine archaea. However, in other incubation studies, pelagic archaea also were capable of using organic carbon. It has remained unknown what fraction of the total marine archaeal community is autotrophic in situ. If archaea live primarily as autotrophs in the natural environment, a large ammonia-oxidizing population would play a significant role in marine nitrification. Here we use the natural distribution of radiocarbon in archaeal membrane lipids to quantify the bulk carbon metabolism of archaea at two depths in the subtropical North Pacific gyre. Our compound-specific radiocarbon data show that the archaea in surface waters incorporate modern carbon into their membrane lipids, and archaea at 670 m incorporate carbon that is slightly more isotopically enriched than inorganic carbon at the same depth. An isotopic mass balance model shows that the dominant metabolism at depth indeed is autotrophy (83%), whereas heterotrophic consumption of modern organic carbon accounts for the remainder of archaeal biomass. These results reflect the in situ production of the total community that produces tetraether lipids and are not subject to biases associated with incubation and͞or culture experiments. The data suggest either that the marine archaeal community includes both autotrophs and heterotrophs or is a single population with a uniformly mixotrophic metabolism. The metabolic and phylogenetic diversity of the marine archaea warrants further exploration; these organisms may play a major role in the marine cycles of nitrogen and carbon.biomarkers ͉ carbon isotopes ͉ microbial ecology ͉ nitrogen cycle ͉ oceanography N onthermophilic archaea represent up to 40% of the free-living prokaryotic community in the water column of the world's oceans (1-6), but until recently there has been limited information about the sources of carbon and energy that fuel these organisms (7-11). The characteristic membrane lipids of planktonic archaea include glycerol dialkyl glycerol tetraethers (GDGTs) (12). These compounds are ubiquitous in marine sediments and ocean water (12-15). The relative abundance of individual GDGTs recovered from sediments is used to reconstruct sea-surface temperatures (16)(17)(18). This distribution, known as TEX 86 , has been shown through experimental manipulation of surface-water mesocosm experiments to respond to changes in incubation temperature (18). In addition, the ␦ 13 C values of GDGTs display a remarkably constant offset from ␦ 13 C values of dissolved inorganic carbon (DIC) over a range of settings and geologic time (13,(19)(20)(21). The collective metabolic activities of the numerous archaea in the ocean are likely to play a significant role in the cycling of organic carbon (OC) and nutrients, and their membrane lipids show significant utility for paleoceanography. However, neither the metabolic requiremen...

Crenarchaea and phytoplankton coupling in sedimentary archives: Common trigger or metabolic dependence?

“…It is possible that ammonium-oxidizing chemoautotrophic Crenarchaea might also be attached to degrading phytoplankton particles using up the released ammonium. If Crenarchaea are heterotrophs, ammonium-oxidizing chemoautotrophs, or majorly mixotrophs (Hallam et al 2006;Ingalls et al 2006), crenarchaeal abundance changes might follow phytoplankton productivity patterns with a delay if Crenarchaea do not rely on resources released by exudation but by cell lysis or indirectly by egestion from phytoplankton grazers. Such delay, or seasonal succession, might cause the decoupling found between phytoplankton and Crenarchaea in snapshot water-column samples, but will be smoothed out in our time-integrated sedimentary material.…”

“…Different dominant metabolic pathways have been suggested to operate in Archaea, notably heterotrophy (Ouverney and Fuhrman 2000; Teira et al 2006) and also mixotrophy utilizing both CO 2 and organic carbon (Hallam et al 2006;Ingalls et al 2006). Other studies suggest that Crenarchaea can be chemoautotrophs with light-independent inorganic carbon fixation metabolism (Pearson et al 2001;Herndl et al 2005), but their energy source remained unknown until Könneke et al (2005) grew a pure Crenarchaea culture on ammonium and CO 2 alone.…”

Towards a better understanding of microbial carbon flux in the sea*

“…Since deep-ocean bacteria are generally limited by the availability of organic carbon, it can be deduced with reasonable certainty that the anaplerotic metabolism of heterotrophic bacteria is only of minor importance. In contrast, deep-water chemoautotrophy by prokaryotes has not received adequate attention and has only sporadically been measured, but recent data suggest that it might be far more important than hitherto assumed , Ingalls et al 2006). While our knowledge of the spatial distribution and magnitude of carbon fixation in the oxygenated dark realm, comprising ca.…”

“…As nitrifying prokaryotes use inorganic carbon as a carbon source, the nitrifying prokaryotes, and particularly Crenarchaeota, represent a major source of newly synthesized organic carbon, i.e. an organic carbon source not transformed from phytoplankton (Ingalls et al 2006).…”

Intact polar and core glycerol dibiphytanyl glycerol tetraether lipids in the Arabian Sea oxygen minimum zone. Part II: Selective preservation and degradation in sediments and consequences for the TEX86

“…GDGTs are preserved well in the sedimentary record and can thus be used as biomarkers for this group of Archaea (e.g. Kuypers et al, 2001;Pancost et al, 2001;Ingalls et al, 2006;Coolen et al, 2007). Schouten et al (2002) found a correlation between sea surface temperature (SST) and the distribution of four specific GDGTs present in sediment core tops (GDGT-1, -2, -3 and -4 0 , Fig.…”