Massive Expansion of Marine Archaea During a Mid-Cretaceous Oceanic Anoxic Event

Kuypers, Marcel M. M.; Blokker, Peter; Erbacher, Jochen; Kinkel, Hanno; Pancost, Richard D.; Schouten, Stefan; Damsté, Jaap S. Sinninghe

doi:10.1126/science.1058424

Cited by 240 publications

(156 citation statements)

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“…Gene copies at 450 m were comparable to those in the upper portion of the water column, and reached 10 4 copies per milliliter in the Carmen Basin. Relatively high archaeal amoA abundances under suboxic conditions are in line with a number of previous studies: expansions of marine archaea may occur during oceanic anoxic events (Kuypers et al, 2001), archaeal amoA genes have been recovered from the OMZ of the ETNP and from the suboxic zone of the Black Sea (Francis et al, 2005), and archaeal amoA copy numbers were maximal in the suboxic zone of the Black Sea (Coolen et al, 2007;Lam et al, 2007). In an interesting parallel, the distribution of marine Crenarchaeota based on their membrane lipid, crenarchaeol, showed consistently high abundances at 450 m in the OMZ of the Arabian Sea (Sinninghe Damste et al, 2002).…”

Section: Resultssupporting

confidence: 91%

“…In particular, although marine Crenarchaeota have been shown to numerically dominate microbial communities throughout the water column (DeLong et al, 1994;Karner et al, 2001), there has been limited insight into the biogeochemical and ecological roles of these organisms following their initial identification in the ocean (DeLong, 1992;Fuhrman et al, 1992;Francis et al, 2007). Consistent with a role in nitrification-the stepwise oxidation of ammonia (NH 3 ) to nitrite (NO 2 À ) to nitrate (NO 3 À )-several studies have indicated that a large proportion of the Crenarchaeota are autotrophic (Kuypers et al, 2001;Pearson et al, 2001;Wuchter et al, 2003;Ingalls et al, 2006;Kirchman et al, 2007). Most convincingly, cultivation of the autotrophic ammonia-oxidizing archaeon (AOA) Nitrosopumilus maritimus confirmed that at least some mesophilic Crenarchaeota are capable of ammonia oxidation (Kö nneke et al, 2005), and archaeal amoA genes appear to be widespread in water columns and sediments where nitrification is expected to be important (Francis et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

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Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California

2008

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Nitrification plays an important role in marine biogeochemistry, yet efforts to link this process to the microorganisms that mediate it are surprisingly limited. In particular, ammonia oxidation is the first and rate-limiting step of nitrification, yet ammonia oxidation rates and the abundance of ammoniaoxidizing bacteria (AOB) have rarely been measured in tandem. Ammonia oxidation rates have not been directly quantified in conjunction with ammonia-oxidizing archaea (AOA), although mounting evidence indicates that marine Crenarchaeota are capable of ammonia oxidation, and they are among the most abundant microbial groups in the ocean. Here, we have directly quantified ammonia oxidation rates by 15 N labeling, and AOA and AOB abundances by quantitative PCR analysis of ammonia monooxygenase subunit A (amoA) genes, in the Gulf of California. Based on markedly different archaeal amoA sequence types in the upper water column (60 m) and oxygen minimum zone (OMZ; 450 m), novel amoA PCR primers were designed to specifically target and quantify 'shallow' (group A) and 'deep' (group B) clades. These primers recovered extensive variability with depth. Within the OMZ, AOA were most abundant where nitrification may be coupled to denitrification. In the upper water column, group A tracked variations in nitrogen biogeochemistry with depth and between basins, whereas AOB were present in relatively low numbers or undetectable. Overall, 15 NH 4 þ oxidation rates were remarkably well correlated with AOA group A amoA gene copies (r 2 ¼ 0.90, Po0.001), and with 16S rRNA gene copies from marine Crenarchaeota (r 2 ¼ 0.85, Po0.005). These findings represent compelling evidence for an archaeal role in oceanic nitrification.

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Section: Resultssupporting

confidence: 91%

Section: Introductionmentioning

confidence: 99%

Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California

2008

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“…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.…”

Section: Introductionmentioning

confidence: 99%

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

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Hopmans

Reichart

et al. 2012

Geochimica et Cosmochimica Acta

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The TEX 86 is a proxy based on a ratio of pelagic archaeal glycerol dibiphytanyl glycerol tetraether lipids (GDGTs), and used for estimating past sea water temperatures. Concerns exist that in situ production of GDGTs lipids by sedimentary Archaea may affect its validity. In this study, we investigated the influence of benthic GDGT production on the TEX 86 by analyzing the concentrations and distributions of GDGTs present as intact polar lipids (IPLs) and as core lipids (CLs) in three sediment cores deposited under contrasting redox conditions across a depth range from 900 to 3000 m below sea level in and below the Arabian Sea oxygen minimum zone (OMZ). Direct analysis of IPLs with crenarchaeol as CL via HPLC/ESI-MS 2 revealed that surface sediments in the OMZ were relatively depleted in the phospholipid hexose, phosphohexose (HPH)-crenarchaeol compared to suspended particulate matter from the water column, suggesting preferential and rapid degradation of this IPL. In sediment cores recovered from deeper, more oxic environments, concentrations of HPH-crenarchaeol peaked at the surface, probably due to in situ production by ammonia-oxidizing Archaea, followed by a rapid decrease with increasing depth. No surface maximum was observed in the sediment core from within the OMZ. In contrast, the glycolipids, monohexose-crenarchaeol and dihexose-crenarchaeol, did not change in concentration with depth in the sediment, indicating that they were relatively well preserved and likely mostly derived from fossil pelagic GDGTs. These results suggest that phospholipids are more sensitive to degradation, while glycolipids might be preserved over longer time scales, in line with previous incubation and modeling studies. Furthermore, in situ produced IPL-GDGTs did not accumulate as IPLs, and did not influence the CL-TEX 86 . This suggests that in-situ produced GDGT lipids were more susceptible to degradation than fossil CL and IPL and did not accumulate as CL. In agreement, no significant changes of TEX 86 with sediment depth in the core lipids were observed. However, consistent differences between IPL-derived TEX 86 and CL-TEX 86 were found. These could be explained by a different composition of CL-GDGT of the glyco-and phospholipids, in combination with dissimilar degradation rates of phospholipids vs. glycolipids. We also observed consistent differences in both IPL-derived and CL-TEX 86 between the different cores, equivalent to 3°C when converted to temperature, despite the proximity of the core locations. These differences may potentially be due to a larger addition of GDGTs produced in deeper, colder waters to the (sub)surface-derived GDGTs for the deeper core sites.

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“…Upon cell death, most of these intact polar lipids (IPLs) are transformed into core lipids (CLs) via hydrolysis of the polar head groups (White et al, 1979). This supposedly rapid loss of functional groups resulted in their use as suitable markers for living cells, in contrast to the core lipids, which can be preserved over geological timescales of millions of years (e.g., Kuypers et al, 2001;Jenkyns et al, 2012). Considerable amounts of IPL GDGTs (10 -10 000 ng g -1 sediment) were found in shallow to deeply buried marine sediments [0.7 to 121 m below sea floor (mbsf)], which suggests the presence of a large number of living archaeal cells (Biddle et al, 2006;Lipp et al, 2008;Lipp and Hinrichs, 2009).…”

Section: Introductionmentioning

confidence: 99%

Differential degradation of intact polar and core glycerol dialkyl glycerol tetraether lipids upon post-depositional oxidation

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Kraaij

Tjallingii

et al. 2013

Organic Geochemistry

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Archaeal and bacterial glycerol dialkyl glycerol tetraether lipids (GDGTs) are used in various proxies, such as TEX 86 and the BIT index. In living cells, GDGTs contain polar head groups (intact polar lipids -IPLs). IPL GDGTs have also been detected in ancient marine sediments and it is unclear whether or not they are fossil entities or are part of living cells. In order to determine the extent of degradation of IPL GDGTs over geological timescales, we analyzed turbidite deposits, which had been partly reoxidized for several kyr after deposition on the Madeira Abyssal Plain. Analysis of core lipid (CL) and IPL-derived GDGTs showed a reduction in concentration by two orders of magnitude upon post-depositional oxidation, while IPL GDGTs with a mono-or dihexose head group decreased by 2-3 orders of magnitude. The BIT index for CL-and IPL-derived GDGTs increased substantially upon oxidation from 0.1 to up to 0.5. Together with changing MBT/ CBT values, this indicates preferential preservation of soil-derived branched GDGTs over marine isoprenoid GDGTs, combined with in situ production of branched GDGTs in the sediment. The TEX 86 value for IPL-derived GDGTs decreased by 0.07 upon oxidation, while that of CL GDGTs showed no significant change. Isolation of IPLs revealed that the TEX 86 value of monohexose GDGTs was 0.55, while the TEX 86 value for dihexose GDGTs was substantially higher, 0.70. Thus, the decrease in TEX 86 for IPL-derived GDGTs was in agreement with the dominance of monohexose GDGTs in the oxidized turbidite, probably caused by a combination of in situ production as well as selective preservation of terrestrial isoprenoid GDGTs. Due to the low amount of IPL GDGTs vs. CL GDGTs, the impact of IPL degradation on CL-based TEX 86 paleotemperature estimates is negligible.

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Massive Expansion of Marine Archaea During a Mid-Cretaceous Oceanic Anoxic Event

Cited by 240 publications

References 20 publications

Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California

Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California

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

Differential degradation of intact polar and core glycerol dialkyl glycerol tetraether lipids upon post-depositional oxidation

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