Archaea in organic-lean and organic-rich marine subsurface sediments

26 Pages·2012·2.01 MB·English

by  Andreas Teske

HYPOTHESISANDTHEORYARTICLE
published:31May2012
doi:10.3389/fmicb.2012.00168
Archaea in organic-lean and organic-rich marine
subsurface sediments: an environmental gradient reflected
in distinct phylogenetic lineages
AlanM.Durbin1 andAndreasTeske2*
1DepartmentofEcologyandEvolutionaryBiology,UniversityofCaliforniaIrvine,Irvine,CA,USA
2DepartmentofMarineSciences,UniversityofNorthCarolinaatChapelHill,ChapelHill,NC,USA
Editedby: Examining the patterns of archaeal diversity in little-explored organic-lean marine subsur-
VirginiaP.Edgcomb,WoodsHole facesedimentspresentsanopportunitytostudytheassociationofphylogeneticaffiliation
OceanographicInstitution,USA
and habitat preference in uncultured marine Archaea. Here we have compiled and re-
Reviewedby:
analyzedpublishedarchaeal16SrRNAclonelibrarydatasetsacrossaspectrumofsediment
PeterD.Countway,Bigelow
LaboratoryforOceanSciences,USA trophicstatescharacterizedbyawiderangeofterminalelectron-acceptingprocesses.Our
JulieA.Huber,MarineBiological results show that organic-lean marine sediments in deep marine basins and oligotrophic
Laboratory,USA open ocean locations are inhabited by distinct lineages of archaea that are not found
*Correspondence: in the more frequently studied, organic-rich continental margin sediments.We hypothe-
AndreasTeske,DepartmentofMarine
size that different combinations of electron donor and acceptor concentrations along the
Sciences,UniversityofNorthCarolina
atChapelHill,3117BVenableHall,CB organic-rich/organic-leanspectrumresultindistinctarchaealcommunities,andproposean
3300,ChapelHill,NC27599,USA. integratedclassificationofhabitatcharacteristicsandarchaealcommunitystructure.
e-mail:[email protected]
Keywords:archaea,marinesediments,oligotrophy,subsurface,phylogeny,unculturedarchaea
INTRODUCTION 2008; Sørensen and Teske, 2006; Teske and Sørensen, 2008; Fry
Marine sedimentary microbial communities are key mediators etal.,2008).TheseincludetheMarineBenthicGroupB(MBG-
ofglobalbiogeochemicalcycles(e.g.,D’Hondtetal.,2002,2004; B,Vetrianietal.,1999),adeeplybranchingphylum-levellineage;
Wellsburyetal.,2002).TheDomainArchaeaaccountsforalarge the Miscellaneous Crenarchaeotal Group (MCG, Inagaki et al.,
portion,perhapsthemajority,ofdeep-subsurfaceprokaryoticcells 2003),afrequentlydetectedcrenarcheotallineagewithhighintra-
andbiomass(Biddleetal.,2006;Lippetal.,2008),andbyimpli- group diversity; the South African Gold Mine Euryarchaeotal
cation,globalbiomass(Parkesetal.,1994;Whitmanetal.,1998). Group (SAGMEG, Takai et al., 2001); and the Marine Benthic
Themajorityofstudiesthusfarhavefocusedonrelativelyorganic- GroupD(MBG-D,Vetrianietal.,1999),aeuryarchaeotalgroup
richdeep-subsurfacesediments(e.g.,Parkesetal.,1994,2005;Reed affiliated with the Thermoplasmatales. All of these are approx-
etal.,2002;Wellsburyetal.,2002;D’Hondtetal.,2004;Biddleetal., imately phylum-level in divergence, with the exception of the
2006;Inagakietal.,2006;SørensenandTeske,2006;Kendalletal., MBG-D,which groups along with the MG-II archaea (DeLong,
2007;Heijs et al.,2008;Nunoura et al.,2008). However,abyssal 1992;Fuhrmanetal.,1992)andMG-IIIarchaea(Fuhrmanand
sediments >2000m water depth cover a much larger extent of Davis, 1997) in a well-supported clade affiliated with the Ther-
the ocean floor (∼89%; Dunne et al.,2007) and,in contrast to moplasmatales (Durbin and Teske,2011). However,our current
marginorcoastalsediments,aregenerallyoligotrophic,withlow datasets on archaeal community composition in deep marine
organiccarboncontent(<1%)andslowratesofdeposition(Seiter sedimentsarebiasedtowardorganic-richcontinentalmarginsed-
etal.,2004;Dunneetal.,2007).Electronacceptorssuchasoxy- iments (Teske and Sørensen, 2008). Relatively few studies have
gen or nitrate penetrate these oligotrophic sediments on a scale surveyedthearchaealdiversityofabyssaloroceangyresediments
of meters (D’Hondt et al.,2004) or tens of meters (Gieskes and todate.Amoreorlesscomprehensivelistincludes:Vetrianietal.,
Boulègue,1986;D’Hondtetal.,2009),incontrasttoorganic-rich 1999;Inagakietal.,2001;Sørensenetal.,2004;Wangetal.,2004;
continental margin or shelf sediments where these strong elec- Nercessianetal.,2005;Wangetal.,2005;Xuetal.,2005;Gillanand
tronacceptorsareusedupwithincentimeters.Thisexpansionof Danis,2007;Lietal.,2008;Taoetal.,2008;Rousseletal.,2009;
the oxic and nitrate-reducing zone in oligotrophic sediments is Wangetal.,2010a,Liaoetal.,2011;DurbinandTeske,2010,2011.
afunctionof theslowratesof carbondepositionandmicrobial Mostofthesestudiesarelimitedtoshallowsediments(<1mdeep)
carbonremineralization.Thecombinationofhigher-energyelec- ortofewdepthintervals.Thus,theavailabledatabaseforarchaeal
tron acceptor type and slower flux of electron donor substrates communitiesinoligotrophicmarinesubsurfacesedimentshasnot
likelyimposesdistinctconstraintsonlifeinoligotrophicmarine yetreachedthesamecoverageaseutrophicsediments.Nonethe-
sediments,whichcoverthemajorityofthesurfaceofEarth. less,initial datasets from the South Pacific (Durbin et al.,2009;
Several phylum-level uncultured archaeal lineages have been DurbinandTeske,2010,2011)andotherdatasetsintheliterature
identifiedastypicaldeep-subsurfacesediment-associatedgroups pointtoprofoundlydifferentarchaealcommunities,withlittleor
(Inagakietal.,2003,2006;Parkesetal.,2005;Biddleetal.,2006, nooverlapatthephylumandsubphylumlevel.
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DurbinandTeske Archaeainorganic-leanandorganic-richmarinesediments
Examiningthepatternsofarchaealdiversityinlittle-explored clathrate-bearing deep-subsurface sediments of ODP site 1230
oligotrophicsedimentspresentsanopportunitytostudytheasso- in the Peru Trench (Parkes et al.,2005; Biddle et al.,2006; Ina-
ciationofphylogeneticaffiliationandhabitatpreferenceinuncul- gakietal.,2006;SørensenandTeske,2006),andwithsediments
tured Archaea. We expect a linkage between sediment habitat fromtheCascadiaMarginoffshoreOregonrecoveredduringODP
type and phylogenetic identity, since the distinct physiological Leg 204 (Inagaki et al., 2006; Nunoura et al., 2008). ODP Leg
demands – sustaining metabolism and growth with low-energy 201 Site 1226 south of Galapagos was included as an example
electron acceptors in anaerobic,organic-rich sediments,in con- of a mesotrophic deep marine sediment, and IODP Expedition
trasttoelectrondonorlimitationinoxidizedsediments–should 308 sites U1319 and U1320 were included as examples of tur-
selectfordistinctorganismsinorganic-lean,oxidizedsediments biditecontinentalslopesediments(Nunouraetal.,2009).Methane
thatdifferfromthoseinorganic-rich,reducedsediments.Special- seepsedimentsfromtheMediterraneanprovidedanexampleof
ization in terminal electron acceptors with higher redox poten- a deepwater,yet highly reducing shallow sediment environment
tialforagivensubstratemaydifferentiateorganismsadaptedto (Heijsetal.,2008).Aphylogeneticandenvironmentaloutgroup
oxic/suboxic organic-lean environments from those adapted to is provided by sequences from two non-marine anoxic habitats,
moreorganic-rich,typicallyanoxicenvironments. ananaerobicdigestor(Chouarietal.,2005)andrumen(Sundset
However, an important caveat is that free-energy yield is etal.,2009).
highly contingent on in situ conditions,possibly subverting the Althoughgeochemicaldatawereincomplete,twositesfromthe
expected hierarchy of electron acceptor energy yields based on SouthChinaSea(MD05-2896,MD05-2902;Wangetal.,2010a)
standard conditions. Factors such as syntrophy (McInerney and and several sediment columns from the Coral Sea (ZoNéCo-
Beaty,1988),biotic(Wangetal.,2008,2010b),orabiotic(König 12 sites; Roussel et al., 2009) were included as oligotrophic to
etal.,1997,1999)releasefromfeedbackinhibition,pH(Postma mesotrophicsedimentaryenvironments(Table1;Figure1)based
andJakobsen,1996;Thamdrup,2000),andsubstratecompetitive on nearby ODP sites with complementary geochemistry data.
releaseorsubstrate-pooling(e.g.,Leveretal.,2010)mayallimpact Approx.195kmseparatesODPLeg184Site1148andMD05-2902,
insituenergeticsofmetabolisms.Additionally,redoxnicheadap- botharelocatedatsimilardepths(Site1148:∼3700;MD05-2902:
tationlikelyextendsbeyondsimplytheabilitytouseaparticular ∼3300m) in the Pearl River Basin, Northern South China Sea.
electronacceptor.Insituredoxstate(E )determinesthethermo- ODPLeg184Site1143andMD05-2896areseparatedby∼210km
h
dynamicfavorabilityof agivenbiosyntheticpathway,asbiosyn- within the Dangerous Grounds geologic province of the South
theticpathwaysfeasibleunderhighlyreducedconditionsareless ChinaSea.Althoughthesesitesareatsignificantlydifferentdepths
favorableinmoreoxidizedenvironments;fattyacidbiosynthesis (approx.1650mforMD05-2896and∼2770 mforSite1143),they
(palmitate) is a classic example (McCollom and Amend, 2005). shareacommonsedimentaryregimeofpelagicdrapeamidbroken
Lowsubstrateconcentrationsinorganic-leanenvironmentsmay carbonate platforms distant from the continental shelf (Hutchi-
be countered with high-substrate-affinity catabolic enzymes, as son,2004).AnalogsfortheZoNeCo-12sitesintheFairwayBasin
intheoligotrophicarchaeonNitrosopumilusmaritimus(Martens- south of New Caledonia come from a prior geochemical survey
Habbenaetal.,2009).Economicaluseofelectronacceptorswitha (ZoNéCo-5)of thesamemarinebasin.Thesitesfromthesetwo
highredoxpotential,asshownforammonia-oxidizingThaumar- surveys are ∼127 to 285km distant, and are located at similar
chaeota(SchleperandNicol,2010),mayalloworganismstotake depths (ZoNeCo-5: 2700m; ZoNeCo-12: ∼2500–2700m), with
advantageoftheexpandedredoxtransitionzonesinorganic-lean presumablysimilarsedimentationregimes(Dickensetal.,2001).
environments. Someoligotrophicsedimentsareproblematicsincetheirmicro-
With the largely unexplored complexity of organismal redox bialcommunitystructureandgeochemicalcharacteristicsoverlap
adaptationnoted,wehypothesizethatdifferentcombinationsof withthoseofhydrothermalsediments(Inagakietal.,2001;Ner-
electron donor and acceptor concentrations along the organic- cessian et al.,2005; Li et al.,2008) and the deep-water column.
rich/organic-leanspectrumresultindistinctarchaealcommuni- Several studies of oligotrophic abyssal sediments (Wang et al.,
tiesthathaveoptimizedtheirenergeticrequirementsforcellmain- 2004;Xuetal.,2005;GillanandDanis,2007)sampledonlysurficial
tenanceandgrowth.Thishypothesisarticleexaminespublished sediments and recovered the same archaeal phylum,the Marine
archaeal16SrDNAclonelibrarydatasetsacrossawidespectrumof GroupICrenarchaeota,thatispresumeddominantintheoverly-
sedimenttrophicstatesandterminalelectron-acceptingprocesses. ing water column (e.g.,Karner et al.,2001; Church et al.,2003;
Agogué et al., 2008; Durbin and Teske, 2010). Because of the
SAMPLINGSITES highpotentialforcross-contaminationandthephylogeneticsim-
Thisstudyanalysesarchaealcommunitiesinorganic-leansubsur- ilarity between oxic sediments and the overlying water column,
face sediments from the South China Sea (Wang et al., 2010a), to confidently label MG-I clones collected from oxic sediments
theFairwayBasinintheWesternTropicalPacific(Rousseletal., as indigenous requires stringent contamination controls and/or
2009), the Peru Basin offshore Peru (Sørensen et al., 2004), the investigationsof thediversityof contaminationsources(Durbin
equatorial upwelling zone west of the Galapagos (Teske, 2006; andTeske,2010).Duetothesedifficulties,MG-Isequenceswere
Teske and Sørensen, 2008), and the South Pacific Subtropical excludedfromthecurrentanalysis.
FrontnortheastofNewZealand(DurbinandTeske,2011;Table1;
Figure1).Thesesedimentswerecontrastedwithorganic-richsed- THESEDIMENTARYTROPHICSTATESPECTRUM
imentsofODPLeg201sites1227and1229,locatedbeneaththe In the following section, we summarize some of the most
highly productive Peruvian upwelling zone, with the methane- informative biogeochemical and microbiological parameters for
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DurbinandTeske Archaeainorganic-leanandorganic-richmarinesediments
Reference D’Hondtetal. (2009),Durbin andTeske (2010) D’Hondtetal. (2009),Durbin andTeske (2011) Shipboard ScientificParty (2003f), D’Hondtetal. (2004), *Shipboard ScientificParty (1976) Shipboard ScientificParty (2003a), *Shipboard ScientificParty (1992a) (Continued)
/ d
e e s
Sulfid reduc metal −−/ −+/ −+/ −+/
Sulfate concentration minima[mM] anddepth [mbsf] Nodepletion Nodepletion Nodepletion Nodepletion
sediments. Nitrate depletion depth, mbsf No depletion 2.55 0.1–0.4 ∼1.5
e
subsurfac Oxygen depletion depth, mbsf No depletion ∼0.70 Nodata Nodata
e
c-richmarin Ammonia,μM Below detection Below detection 7.64–32.72 6.15–38.48
ni
antoorga Max. DIC, mM 2.44mEq (alkalinity) 3.23mEq (alkalinity) 3.64 3.98
e
oforganic-l TOC,% weight of sediment 0.51 (0.0–0.05 mbsf) 0.34 (0.0–0.05 mbsf) 0.07–0.7 0.00– 0.53
totrophicstate Sedimentation rate,m/My [DSDP/ODP site] 0.9[averaged overentire sediment column] 1.8[averaged overentire sediment column] Closestanalog: Eocene- Quaternary,4-10 [DSDP321]* Closestanalog: Miocene- Quaternary, 15–65[ODP 851]*
g
n
metersrelati Log[10] range, and mbsf rangeof cell counts 3.87–6.63 [2.96–0.1] 5.37–6.3 [4.9–0.25] 5.14–8.24 [81.64–0.01] 5.26–6.87 [320–0.85]
a
sticsandpar Length ofcored Sediment andtotal sediment thickness, mbsf 2.98[67] 4.98[130] 119.1∼[120] 315.6∼[320]
aracteri Water depth 5076 5306 4813 3760
h
c
viewofsite Marine Province, location South PacificGyre 41˚51.13S, 153˚06.38W South Pacific Subtrop. Front 45˚57.86S, 163˚11.05W PeruBasin 12˚01.29S, 81˚54.24W Eastern Equat. Pacific 02˚46.22N, 110˚34.30W
er
v
O
Table1| Site SPG11 SPG12 ODPLeg 201,site 1231 ODPLeg 201,site 1225
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DurbinandTeske Archaeainorganic-leanandorganic-richmarinesediments
Reference Shipboard ScientificParty (2003b), *Shipboard ScientificParty (1992b) Wangetal. (2010a),*ODP Leg184: Shipboard ScientificParty (2000b) Wangetal. (2010a),*ODP Leg184: Shipboard ScientificParty (2000a) Rousseletal. (2009), *Dickensetal. (2001) Expedition308 Scientists (2006b)
/ d
e e s
Sulfid reduc metal ++/ ++/ ++/ ++/ ++/
Sulfate concentration minima[mM] anddepth [mbsf] Partial depletion (18.9mMat 246mdepth) Closest analog:3mM at630–650m [ODP1148]* Closest analog: 6.3mMat500 mbsf[ODP 1143]* 18mMat7.5 mbsf Extrapolated depletion depthat3022:∼60m Depletionto 0.6mMat 22mbsf
n
Nitrate depletio depth, mbsf Not resolved Nodata Nodata Nodata Nodata
n
Oxygen depletio depth, mbsf Nodata Nodata Nodata Nodata Nodata
Ammonia,μM 51.7–641 Closest analog: 640-1390 [ODP 1148]* Closest analog: 200–1900 [ODP 1143]* Nodata 132–3816
y]
Max. DIC, mM 7.03 Closest analog: 9.14 [ODP 1148]* Closest analog: 11.18 [ODP 1143]* Nodata 15.99 [alkalinit
TOC,% weight of sediment 0.25–3.49 0.2–1.4 0.2–1.3 Nodata 0.03–1.99
Sedimentation rate,m/My [DSDP/ODP site] Closestanalog: Miocene- Quaternary,∼40[ODP 846]* Closestanalog: Miocene,11–17 Plioceneto Pleistocene, 27–63[ODP 1148]* Closestanalog: Mioceneto recent,30–50 [ODP1143]* Closestanalog: Neogene,10 [ZoNeCo-5sites inFairway Basin]* 1810[Holocene to80ky]
1] 5]
Log[10] range, and mbsf rangeof cell counts ∼6–8.67 [420–0.0 Nodata Nodata 6.2–8.3 [9.4–0.2] <4–6.08 [284.8–7.
Length ofcored Sediment andtotal sediment thickness, mbsf 418.9[421] >9.42[850] 11.03>[500] 9.4>>[560] 299.6
Water depth 3297 3697 1657 2294 (MD06- 3022),∼2700 others 1480
ntinued Marine Province, location South Equat. Current near Galapagos 03˚05.80S, 90˚49.07W South ChinaSea, PearlRiver Basin 17˚57.70N, 114˚57.33E Southern, South ChinaSea 08˚49.59N, 111˚26.47E Fairway Basin,Coral Sea24˚S, 163˚E Brazos Basin 27˚18.08N, 94˚23.25W
Table1|Co Site ODPLeg 201,site 1226 MD05-2902 NorthCore MD05-2896 SouthCore ZoNeCo-12: MD06- 3022, MD063026, MD063027, MD063028 IODPleg 308,site U1320
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DurbinandTeske Archaeainorganic-leanandorganic-richmarinesediments
Expedition308 Scientists (2006a) Shipboard ScientificParty (2003c) *Shipboard ScientificParty (1988a) Shipboard ScientificParty (2003d) *Shipboard ScientificParty (1988b) Shipboard ScientificParty (2003e) *Shipboard ScientificParty (1988c) Shipboard ScientificParty (2003g) *Nunoura etal.(2008) (Continued)
+ + + + +
+/ +/ +/ +/ +/
Depletionto 0.5mMat15 mbsf Depletionat∼41mbsf Depletionat∼32mbsf Depletionat∼9mbsf Depletionto∼0.5–1mMat∼11mbsf
ata ved ved ved ata
Nod Not resol Not resol Not resol Nod
a a a a a
at at at at at
d d d d d
o o o o o
N N N N N
1
291–441 3168.2– 8875.5 5335.69– 6746.53 1920– 40170 Max. 22700
y] y]
nit 5 nit
19.45 [alkali 25.78 21.14 162.9 68.9 [alkali
0.16–1.9 1.16– 10.57 0.83–3.97 1.27–3.98 0.87–1.75
e} 80 P
150[Holocen 2310>[90–150ky] Miocene- Quaternary: 20-50[ODP 684]* ∼Quaternary [ODP681]* Miocene- Quaternary: 100–250[OD 685]* 60–270
<4–6.08 [157.5–4.4] 6.25–7.70 [151-0.15] 6.43–9.97 [185.7– 90.45] 6.1–8.62 [257.7–0.01] ∼6–7,qPCR [123–2.0]*
>) >>) >>) >)
7.5 >1( 2.9( 7.3( >0(
5 5 9 7 8
1 1 1 2 3
0 6
4 7 1 8 0
4 2 5 0 9
1 4 1 5 8
Brazos Basin 27˚15.96N, 94˚24.19W PeruMargin 08˚59.45N, 79˚57.35W PeruMargin 10˚58.57S, 77˚57.46W PeruTrench 09˚06.78S, 80˚35.01W Cascadia Margin 44˚35.18N, 125˚07.19W
IODPleg 308,site U1319 ODPLeg 201,site 1227 ODPLeg 201,site 1229 ODPLeg 201,site 1230 ODPLeg 204,site 1244
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DurbinandTeske Archaeainorganic-leanandorganic-richmarinesediments
Reference Shipboard ScientificParty (2003h) *Nunoura etal.(2008) Shipboard ScientificParty (2003i) *Nunoura etal.(2008) Heijsetal. (2008) Heijsetal. (2008)*Kor- masetal. (2008) Heijsetal. (2008) ODP1226,South dNHporewater4
Sulfide/ reduced metals ++/ ++/ +/nodata +/nodata +/nodata ophicsites( highDICan
otr by
Sulfate concentration minima[mM] anddepth [mbsf] Depletionto∼0.5–1mMat∼8mbsf Depletionto∼0.5-1mM∼at3mbsf Notresolved Depletionat 0.35–0.40 mbsf [0.25mbsf]* Notresolved 5and1231);mes 51)characterized
2 2
NitrateOxygen depletiondepletion depth,depth, mbsfmbsf NodataNodata NodataNodata Nodata0cmbsf ∼Nodata6cmbsf Nodata0cmbsf meters(SPG12,ODP12 204sites1244,1245,1
Ammonia,μM Max. 21800 Max. 14800 217.2–40.6 30.0–158.5 50.6–152.5 epletionwithin 1230;ODPLeg
Max. DIC, mM 73.31 [alkalinity] 122.37 [alkalinity] Nodata Nodata Nodata withnitrated s1227,1229,
s e
TOC,%SedimentationLog[10] weightrate,m/Myrange, of[DSDP/ODPand sedimentsite]mbsf rangeof cell counts 100–6200.71–1.46Not detectedin qPCR* ∼600–16000.58–3.066–8, qPCR [204.2– 4.5]* NodataNotapplicable1.22–3.95 NodataNotapplicable2.59–17.4 NodataNotapplicable3.9–4.31 etionofoxygenornitrate(SPG11);oligotrophicsite sitesU1319,U1320withcaveats;ODPLeg201sit Outgroup,Mediterraneanseepsediments.
Length ofcored Sediment andtotal sediment thickness, mbsf >>540() >>445() >>0.28() >>0.34() >>0.31() ewithoutdepl es(IODP308 ntationrates.
Table1|Continued WaterSiteMarine depthProvince, location 870CascadiaODPLeg Margin204,site 44˚35.16N,1245 125˚08.95W 1216CascadiaODPLeg Margin204,site 44˚34.21N,1251 125˚04.44W 1947NapolicoldEastern seepMediter- ranean 33˚43.47N, 24˚42.09E 1720KazanmudEastern volcanoMediter- ranean 35˚26.00N, 30˚33.50E 2050EasternAmsterdam Mediter-mud raneanvolcano 35˚19.85N, 30˚16.85E Fromtoptobottom:ultraoligotrophicsit ChinaSea,CoralSea);andeutrophicsit concentrationmaxima,andhighsedime
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DurbinandTeske Archaeainorganic-leanandorganic-richmarinesediments
FIGURE1|Mapdepictingapproximatelocationofmarinesediment TheIODP308sites(U1319,U1320)arelocatedintheturbiditedepositional
coresdiscussedinthecurrentreview.SPG11occursjustinsidethe Brazos-TrinityBasinonthecontinentalslopeofthenorthernGulfofMexico
southernSouthPacificGyre,whileSPG12liesonthesubtropicalfront (Nunouraetal.,2009).TheODPLeg201Sites(ShipboardScientificParty,
separatingthegyrefromtheSouthernOcean(D’Hondtetal.,2009).Sites 2003a–f;D’Hondtetal.,2004)includesitesfromtheeasternequatorial
MD05-2896andMD05-2902(Wangetal.,2010a)arefromtheSouthChina upwellingregion(1225),SouthEquatorialCurrent(1226),PeruMargin(1227,
Sea,withadditionalgeochemicaldataonthesesitessourcedfromnearby 1229),PeruTrench(1230),andthePeruBasin(1231).TheODPLeg204
ODPLeg184Sites1143and1148(ShipboardScientificParty,2000a,b).The CascadiaMarginsitesincludesites1244,1245,and1251(Nunouraetal.,
ZoNéCo-12siteslieintheFairwayBasinintheCoralSea(Rousseletal., 2008).Mudvolcano/coldseepsitesarerepresentedbythreeexamplesfrom
2009),withadditionalinformationfromZoNéCo-5sites(Dickensetal.,2001). theeasternMediterranean(Heijsetal.,2008).
oligotrophicmarinesubsurfacesediments(Table1)andshowthat ultraoligotrophicgyresediments.AnextremeoutlieraretheGulf
thesesitesappeartofallintoseveralnaturalgroups. ofMexicoslopeturbiditesedimentssampledonIODPExpedition
308(Table1).
SEDIMENTATIONRATES
Sedimentation rates can approximate sediment trophic states, POREWATERDIC
albeit with some exceptions for high-carbonate or turbidite- ConcentrationsofporewaterDICaboveorbelowthemeanseawa-
associatedsedimentationandchangingoceanographicconditions terconcentrationareanindicatorofthemagnitudeanddirection
in the surface ocean, which can all enrich or impoverish deep of netmetabolism. Netheterotrophyduetoremineralizationof
marinesedimentsrelativetotheexpectedtrophicstatebasedon organic matter to CO increases DIC concentrations,at least at
2
surfaceoceanproductivity,orifasignificantfractionofsedimen- themoreoligotrophicendofthescale;inhighlyorganic-richsed-
tation is inorganic carbonate or silicate. Sedimentation rates at iments,alargefractionoforganiccarbonmayberemineralizednot
SPG Sites 11 and 12, are near 0.9 and 1.8m/My, averaged over toCO buttomethane.Nevertheless,becauseDICdirectlyreflects
2
theentiredepthandageofthesedimentcolumn(D’Hondtetal., metabolicrates,itintegratesoverunknownsinherentininterpret-
2009).Forreference,averagedoceansedimentationratesforthe ing sedimentation rates or electron acceptor depletion profiles.
Atlantic,Pacific,andIndianOceanbasedonDSDPcoresranged ComparisonsofmaximumDICforLeg201sitessuggestaspec-
from30to50m/myforquaternarysediments,anddecreasedto trumfromhighlyDIC-enrichedCascadiaMarginsites1244,1245,
2–5m/myforpaleocenesediments(WhitmanandDavis,1979). and1251andPeruTrenchSite1230,toPeruMarginsites1229and
AmongODPLeg201sites,Site1231istheslowest-accumulating 1227,theGulfofMexicoExpedition308sites,theSouthChinaSea
site,but still 4 to 10 times or 2 to 5 times faster than the South sites,toODPsites1226,1225,and1231;theSPGsites12and11
Pacific sites SPG11 or SPG12 (Table 1). The Peru Margin,Peru marktheDIC-poorendofthespectrum(Table1).Here,alkalin-
Trench,andCascadiaMarginsitesformacohortwithincreasingly ity(∼96%ofwhichisDIC,atseawaterpH)remainsatseawater
high sedimentation rates, up to 1600m/my at Cascadia Mar- valuesthroughoutthesampledsedimentcolumnatSPG11,while
gin site 1251 (Table 1), three orders of magnitude higher than SPG12displaysadowncorealkalinityincreaseconcomitantwith
at the South Pacific sites (Table 1),dramatically illustrating the oxygendrawdown,andstabilizingthereafter(Table1).Maximal
differentconstraintsshapingeutrophicmarginenvironmentsand porewaterNH concentrationsshowthesametrendandsortthe
4
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DurbinandTeske Archaeainorganic-leanandorganic-richmarinesediments
sitesintothesamesequenceasporewaterDIC(Table1),reflecting sediments, oxidants retreat toward the seawater/sediment inter-
theoriginofNH fromremineralizationofburiedbiomass. face, leading to a shrinking zone of oxidant availability. The
4
porewater gradients of the strongest oxidants (oxygen, nitrate)
ORGANICCARBONAVAILABILITY are therefore strongly compressed toward the sediment surface,
Organiccarbonconcentrationisnotadirectlyproportionalmea- whereastheporewaterprofilesofweakeroxidants(oxidizedmet-
sure of sediment trophic state, as substrate lability and organic als, sulfate) extend deeply into the sediment column (D’Hondt
carbon residence time can vary between sediments with similar etal.,2002,2004).
organiccarboncontents.Therefore,trophicstateofthesediment AttheultraoligotrophicSPG11site,oxygendrawdownismin-
canchangewithoutnecessarilyaffectingthesedimentorganiccar- imal and nitrate drawdown is not evident; porewater oxygen
bon percent weight, and organic carbon content between sites remainsat∼160μMat280cmbsf andisunlikelytobedepleted
of possiblydifferenttrophicstatecanoverlap.AmongtheSouth downcore,unless there are deep biotic or abiotic sediment oxy-
PacificGyresites,organiccarboncontentvaluesforSPG11ranged gensinks(D’Hondtetal.,2009).AtsiteSPG12,oxygenbecomes
from0.59to0.45dryweight%overtheupper9cmbsf(centimeter depletednear70cmbsf,andnitrateisdepletedat253–258cmbsf
belowsurface),withlittlechangeaftertheupper2cmbsf;surface (D’Hondt et al., 2009). Oxygen data are not available for ODP
sediments(0–5cmbsf)fromSPG12contained0.34%(D’Hondt sediment cores; sediment cores from ODP sites 1225 and 1231
etal.,2009).AglobalTOCanalysisinmarinesedimentsshowed shownitratedepletiononthescaleof10–40cmbsffor1231,and
that abyssal sediments contain less than or at most 1 weight% ∼150cmbsfforsite1225(Table1).Thesurficial1–2msediment
TOC,closetotheglobalmeanformarinesediments(Seiteretal., horizons,andthenitrateandoxygenporewaterprofilestherein,are
2004);thisisconsistentwiththeoligotrophicsitesinthissurvey. generallylostordisturbedduringODPcoring.Nitrateandoxygen
Higher TOC values in the range of up 1–2% are shared by the profilesincentimeterresolutioncanbeobtainedfromsediment
SouthChinaSeasitesandtheGulfofMexicoturbiditesediments coreswithundamagedsurfacelayers,sampledbysubmersibleor
(Table1).TheeutrophicLeg201sitesvariedbetween∼1and10% ROV.Forexample,downcorenitratedepletionoccurredbetween
TOCfordifferenthorizons,with∼4%mosttypicalforthemajor- 6 and 22cmbsf for the Kazan mud volcano, and indirect evi-
ityof thesedimentcolumn,andtypicallydecreasingwithdepth dencepointstooxygenpenetrationwithintheupper6cm.Nitrate
(Table1).Interestingly,theCascadiaMarginLeg204sitesshowed remainednear1–2μMintheothertwomudvolcanosites(Ams-
lowerTOCconcentrations(maximaca.1.5–3%)thantheLeg201 terdamandNapoli),andnooxygenpenetrationcouldbeinferred
Peru Margin and Peru Trench sediments,and resembled in this (Heijsetal.,2008).
regardtheGulfofMexicoturbidites(Table1). Sulfate was not measurably drawn down at the SPG12 site,
nor at the oligotrophic ODP sites 1231 and 1225. Mesotrophic
CELLDENSITIES ODPsite1226displayedsulfatedrawdownbutnotdepletionover
TotalprokaryoticcelldensitiesattheSPGsitesarethelowestyet theentiresampledsedimentcolumn,alongwithapparentmetal
recordedforanyequivalentdepthhorizon(D’Hondtetal.,2009). redoxcyclingtoatleast∼70mbsfandmethanogenesisthrough-
Forallsites,cellcountsdeclinedwithsedimentdepth,withthelow- outnearlytheentiresedimentcolumn.Likewise,theODPproxy
estvaluetypicallybeingthedeepest.Cellcountsrangedfrom103.9 sites from the South China Sea revealed sulfate drawdown but
to106.6 permlovertheupper2.8matSPG11,and105.4 to106.3 not depletion over several hundred meters of sediment. Sulfate
permlovertheupper∼5matSPG12,againsettingSPG11apart. profilesfortheshallowCoralSeacoresareincomplete;however,
Thesecellcountswerelowerthanthoseof deepwaterODPsites extrapolatingfromtheupper9msulfateprofileof CoreMD06-
1231and1225atcomparabledepth;thedeepwaterODPsiteshad 3022(Rousseletal.,2009)suggestsaminimumdepletiondepth
similarorhighercellcountsoveramuchbroaderdepthrange,and of 60m or greater. The Gulf of Mexico and Peru Margin sites
declinedtotheirlowestlevelsof∼105atgreaterdepths,81.6mbsf displayedsulfatedepletionwithintensofmeters(D’Hondtetal.,
for1231and320mbsffor1225.Giventheirlocationoncontinen- 2004),thePeruTrenchandCascadiaMarginsitesshowedsulfate
talmargins,theGulfofMexicoturbiditesedimentsofExpedition depletionwithinafewmeters(Table1).Often,porewatersulfate
308hadunusuallylowcelldensities;themaximaintherangeof concentrationsbelowdepletiondepthdonotdecreasetozero,but
105.3 to106.08 cellspermlwerefoundnearthesedimentsurface, fluctuateintherangeof 0.5or1mM,reflectingsulfidereoxida-
and cell densities decreased rapidly with depth (Nunoura et al., tionafterexposureofsulfidiccorestooxygen.InMediterranean
2009).CellcountsofthemesotrophicODP1226andtheeutrophic mudvolcanosediments,sulfatewasdepletedwithinthe∼40cm
Peru Margin and Trench sites ranged from 106 to 1010 cells per measured for the Amsterdam and Napoli mud volcanoes,while
cm3 throughout the sediment column (Table 1). No direct cell theKazanseepdisplayedlittletonodrawdownof sulfate(Heijs
countsareavailablefromtheODP204sites;theqPCRdatafor16S et al.,2008). Geochemical and microbial variability within each
rRNAgenecopynumbershavetobeviewedwithcaution,given mud volcano site is evident from another recent survey of the
occasionallycompletePCRinhibition(Nunouraetal.,2008). Kazanmudvolcano,wheresulfatewasdrawndownwithin25cm
sedimentdepth(Kormasetal.,2008).
OXYGEN,NITRATE,ANDSULFATEGRADIENTS
Typically,electronacceptorsformicrobialmetabolismaredepleted METALREDOXCYCLING
downcore in order of declining energy yield; depletion depth Metal reduction represents a key avenue for anaerobic termi-
increases with organic substrate scarcity. Thus, organic-carbon nal electron-accepting processes (Thamdrup, 2000). Manganese
limited sediments are expected to be deeply permeated by and iron reduction are both typical suboxic processes (Berner,
high-energyelectronacceptors.Withinincreasinglyorganic-rich 1981),withmanganesereductioncomparabletonitratereduction,
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DurbinandTeske Archaeainorganic-leanandorganic-richmarinesediments
andreductionofamorphousironoxyhydroxidesclosertosulfate MexicoExpedition308sitesshowacuriousmixtureofeutrophic
reductioninenergyyield(LovleyandGoodwin,1988).However, characteristics(highDICandNH porewaterconcentrationmax-
4
thefactthatironreductioninvolvesbothsolubleandsolidreac- ima,veryhighsedimentationrates)combinedwithmesotrophic
tants and products,and the different bioavailability of different (lowTOCcontent)orevenoligotrophiccharacteristics(verylow
iron oxide phases,complicate iron geochemistry by introducing cellnumbers).Thefullyeutrophicsedimentsarerepresentedby
additionalcontingentfactors.Theseincludechemicalsurfaceinac- thePeruMargin,PeruTrench,andCascadiaMarginsites.Where
tivation(Fredricksonetal.,1998;Urrutiaetal.,1998;Urrutiaetal., available, DIC and NH porewater concentrations are perhaps
4
1999);retentionofreducedironinclaylattices,whichcounteracts the most reliable trophic state indicators,as they directly reflect
product inhibition of iron reduction (König et al., 1997, 1999) therateandamountofbiomassrecycledbymicrobialcommuni-
andfavorsincreasedinsitufree-energyyieldsforironreduction; ties.MaximumDICvaluesrangefromseawaterconcentrationsfor
andthepHandphasedependenceoffree-energyyields(Postma ultraoligotrophic SPG11,to >10mM for mesotrophic sites,and
and Jakobsen, 1996; Fredrickson et al., 1998), which may result significantlymoreforeutrophicsites(Table1).MaximumNH
4
in higher in situ energy yields for sulfate reduction. In particu- valuesrangefrombelowdetectionfortheultraoligotrophicSPG
lar, precipitation of the reduced byproducts of sulfate and iron sites,to ca. 0.5–2mM for mesotrophic sites,and to >3mM for
reductionresultsinamutualisticpositivefeedbackthatequalizes eutrophicsites(Table1).
energyyieldsforboth(Wangetal.,2008,2010b).Together,these
factors allow recalcitrant metal oxides to persist deep in anoxic PHYLOGENYOFOLIGOTROPHICARCHAEA
zones(D’Hondtetal.,2004;Wangetal.,2008,2010b),whileMn Akeyprobleminsurveyingthearchaealdiversityofmarinesed-
and reactive Fe(III) are mostly reduced nearer to the sediment- iments is reliably defining phylogenetically meaningful groups.
waterinterface(Königetal.,1997;Thamdrup,2000;Wangetal., Longbranchattraction,hyperthermophilehigh-GCconvergence
2008). (Boussau and Gouy, 2006; Brochier-Armanet et al., 2008), and
Sedimentredoxstatecanbecharacterizedbyconsideringiron chimericsequencesinpublicdatabases(HugenholtzandHuber,
andsulfatereductiontogether.Ultraoligotrophic,oxicsiteSPG11 2003;Ashelfordetal.,2005)resultinstatisticallypoorlysupported
shows no evidence of either iron or sulfate reduction (Table1). clades–oftenpara-orpolyphyleticoncloserinspection–thatare
Theanaerobic,oligotrophicsitesSPG12,1225,and1231display highlydependentondetailsofspeciesselection,andhavelittleuse
netironreductionbutnosulfideproduction.Inmesotrophicand inaphylogeneticcontext,butthatareneverthelessreportedinthe
eutrophic sites from the South China Sea, Coral Sea, the Gulf literature.Arelatedcomplicationistheproliferationof different
of Mexico,thePeruMargin,PeruTrench,andCascadiaMargin, namesforequivalentgroupsornearlyequivalentgroups,which
the precipitation of metal sulfides indicates co-occurring sulfate hamperscomparabilityofresults.Asanattempttoaddresssomeof
and iron reduction. Table 1 presents presence/absence patterns thesedifficulties,weconstructedphylogeniesofthemajorarchaeal
forsulfideandreducedmetalsfordifferentsites,usingbothdirect lineages(Figure2),oftheEuryarchaeota(Figures3–5)andCre-
measurement of sulfide (Leg 201 and Mediterranean sites),dis- narchaeota(Figure6),whichreflectthenomenclatureintroduced
solvedporewaterironandmanganese(Leg201,Leg204,andIODP byarangeof studies(Tables2and3).Althoughthesephyloge-
308sediments),aswellasindirectindicatorsforthepresenceor niesdonotaddressthedeeprelationshipsbetweenarchaealphyla,
absenceof reducedsulfurandmetalspecies,suchasameasured such as the placement of Micrarchaeum and Parvarchaeum,and
lack of net sulfate reduction (SPG12, SPG11), the presence of thegroupingofArchaeoglobi,Methanomicrobia,andHalobacte-
authigenic sulfide minerals (Leg 184,Leg 204),or brown–green ria,thesephylogeniesaresimilartowell-supportedcladesreported
colortransitions(Königetal.,1997;Thamdrup,2000)thatarean in previous studies (e.g., Brochier-Armanet et al., 2008; Baker
indicatorofsedimentaryFe(III)/Fe(II)redoxfronts(SPG12,Leg et al., 2010). Particular attention was given to the Thermoplas-
184sites,ZoNéCosites,IODP308sites). mata(Figure5),inanefforttodistinguishphylogeneticallyvalid
clades,alongside the organic-rich-associated MBG-D clade,that
SEDIMENTTROPHICSTATEHIERARCHY occurinoligotrophicsediments.Thephylogeneticstructureofthe
Intermsof electronacceptorgradients,oxygenandnitratepen- unculturedThermoplasmata,andotherhighlydiversifiedgroups,
etration over tens of centimeters to meters, and the absence of suchastheMCGarchaea,remainsaworkinprogress.
sulfatedepletion,characterizetheoligotrophicsitesSPG12,ODP
1231,andODP1225;thelackofoxygendepletionatSPG11sets ARCHAEALOCCURRENCETRENDSACROSSSITES
this ultraoligotrophic site apart. Based on cell densities, nitrate RelativeabundancesofdeeplybranchingArchaeallineagesin16S
and oxygen penetration depth,sedimentation rate,and possibly rRNAgeneclonelibrariesfromoligotrophicandorganic-richsed-
maximumDICvalue,SPG12isthemostorganic-leanamongthe iments are compiled in Figure 7. These 16S rRNA gene clone
oligotrophicsites,whichwouldalsoincludeODPdeepwatersites library data should not be understood as accurate proportional
1231 and 1225. ODP Site 1226 and the South China Sea sites representation of archaeal lineages in the environment; diverg-
displayed sulfate drawdown but not depletion several hundred ingmethodologies,clonelibrarysizelimitationsandtheresulting
metersdeepintothesediment,withtheCoralSeaandtheFairway detection thresholds qualify what is subsequently called“abun-
Basin also possibly in that category, suggesting a“mesotrophic” dance.”High-throughput sequencing approaches are very likely
labelforthesesites.Bycontrast,eutrophicsiteshaveoxygenand tomodifytheseinitialclonelibrary-basedsurveys(Biddleetal.,
nitratepenetrationdepthsofmerecentimeterstomillimeters,and 2008, 2011). Yet, the clone library data provide a window into
sulfate depletion depths of tens of meters or less. The Gulf of distinctly different detection patterns of archaeal clades within
www.frontiersin.org May2012|Volume3|Article168|9
DurbinandTeske Archaeainorganic-leanandorganic-richmarinesediments
Cultured MCG+C3
Caffirelniaatrecdhaeota pUWA2
HWCG−I/
Aigarchaeota
Korarchaeota Group 1.1
pOWA133 pISA7
FnvA51 ASUF3B6T1-12112
pSL22 pISA9
pSL17*
GoC_Arc109 MHVG−2
FnvA65
pMC2A209
MHVG−3
YS18As93*
MBG−B/DSAG DSEG−4*
SM1K20
SBAK−mid−08* DQ078753 pMC2A384
Fhm5A01* Alv−FOS5
VAL II /Eury4
0.10 269986460 Candidatus
Parvarchaeum acidiphilum
DHVE−6
AB293222 Pbsc2A13
Thermoplasmata
DSEG−2*
Methanomicrobia
DHVE−3/DSEG
Archaeoglobi BC07−2A−27/DSEG−3*
ANME−1 DHVE−8 SA2 Group
Methanococci
GoM161_Arch13
SA1
NO27FW Guaymas
Halobacteria EGuroryuaprchaeotal MBG−E MSBL1 HydGC-84-221A MSP41*/Nanohaloarchaea
Methanobacteria
SAGMEG
DHVE−5 Nanoarchaeota
FIGURE2|Phylogeneticcontextofmajorphylumorclass-level wereusedintheanalysisforEuryarchaeotaandCrenarchaeota
lineagesofculturedandunculturedArchaea,asestimatedby together.Certainlineages,suchasMethanopyruskandleri,were
theARBneighbor-joiningalgorithm.Siteswithnucleotidesat excludedduetotheirtendencytoattracthyperthermophilestothe
least60%conservedwithinallEuryarchaeotaincludedinthetree baseofthetree.
organic-leanandorganic-richsediments.Allcladesabsentfrom 1245, 1251), and the highly reducing Mediterranean methane
eutrophic sites,or which occur at less than 1.5% relative abun- seeps, and also in the Gulf of Mexico 308 sites with mixed
dance in any eutrophic site, are colored blue (numbers 1-16 in eutrophic/mesotrophic/oligotrophiccharacteristics.Theseuncul-
Figure7).Thosecladesfoundonlyintheeutrophicend-member tured archaeal lineages that are commonly detected in clone
sites,orwhichoccurinthesesitesatmorethan1.5%frequency,are libraries (Table2) should be congruent with the cren- and eur-
coloredred.Overall,archaealphylathatpredominateeitherinthe yarcheotalproportion(15–45%)of phylogeneticallyinformative
oligotrophicorintheeutrophicendmembersitesaredecliningin pyrosequencingfragmentsinthePeruMarginandBrazosBasin
relativeabundancealongenvironmentalgradientsofredoxstate, metagenomes(Biddleetal.,2008,2011).Thearchaealgroupsthat
organiccarboncontentandbiomassremineralization(Figure7; aretypicallyfoundineutrophicsedimentsalsopersisttoaconsid-
Table1).Dominantbenthicarchaealgroupsoforganic-richsedi- erable extent into organic-leaner sediments. For example,MCG
mentsdisappearinthemostoxidizedsedimentenvironments,and isfoundinallmesotrophicsitesintheSouthChinaSea,Fairway
viceversa. Basin, and ODP site 1226; MBG-B persists in the same sites in
AspecificarchaealassemblageofMBG-B,MCG,SAGMEGand themesotrophicspectrum,andalsoinODPsites1225and1231
MBG-Darchaeaisfoundrepeatedlyintheeutrophicsubsurface (Figure7).Somemembersoftheseandotherarchaealcladesthat
sediments of the Peru Margin (ODP sites 1227,1229), Peru aretypicallyfoundinanaerobic,eutrophicmarinesedimentsalso
Trench (ODP site 1230), Cascadia Margin (ODP sites 1244, occur in reducing,non-marine habitats. For example,the MCG
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