Significance of non-sinking particulate organic carbon and dark CO2 fixation to heterotrophic carbon demand in the mesopelagic northeast Atlantic

Click He e o Full A icle Signi icance o non‐sinking pa icula e o ganic ca bon and da k CO 2 ixa ion o he e o ophic ca bon demand in he mesopelagic no heas A lan ic Fede ico Bal a , 1 Ja ie A ís egui, 1 E a Sin es, 2,4 Josep M. Gasol, 3 Thomas Rein hale , 2,4 and Ge ha d J. He ndl 2,4 Recei ed 2 Ma ch 2010; accep ed 1 Ap il 2010; published 5 May 2010. [1] I is gene ally assumed ha sinking pa icula e o ganic ca bon (POC) cons i u es he main sou ce o o ganic ca bon supply o he deep ocean’s ood webs. Howe e , a majo disc epancy be ween he a es o sinking POC supply (collec ed wi h sedimen aps) and he p oka yo ic o ganic ca bon demand ( he o al amoun o ca bon equi ed o sus ain he he e o ophic me abolism o he p oka yo es; i.e., p oduc ion plus espi a ion, PCD) o deep‐wa e communi ies has been consis en ly epo ed o he da k ealm o he global ocean. While he amoun o sinking POC lux declines exponen ially wi h dep h, he concen a ion o suspended, buoyan non‐sinking POC (nsPOC; ob ained wi h oceanog aphic bo les) exhibi s only small a ia ions wi h dep h in he (sub) opical No heas A lan ic. Based on a ailable da a o he No h A lan ic we show he e ha he sinking POC lux would con ibu e only 4–12% o he PCD in he mesopelagic ealm (depending on he p ima y p oduc ion a e in su ace wa e s). The amoun o nsPOC po en ially a ailable o he e o ophic p oka yo es in he mesopelagic ealm can be pa ly eplenished by da k dissol ed ino ganic ca bon ixa ion con ibu ing be ween 12% o 72% o he PCD daily. Taken oge he , he e is e idence ha he mesopelagic mic ohe e o ophic bio a is mo e dependen on he nsPOC pool han on he sinking POC supply. Hence, he enigma ic majo misma ch be ween he o ganic ca bon demand o he deep‐wa e he e o ophic mic obio a and he POC supply a es migh be subs an ially smalle by including he po en ially a ailable nsPOC and i s au och honous p oduc ion in oceanic ca bon cycling models. Ci a ion: Bal a ,F.,J.A ís egui,E.Sin es,J.M.Gasol,T.Rein hale , and G. J. He ndl (2010), Signi icance o non‐sinking pa icula e o - ganic ca bon and da k CO 2 ixa ion o he e o ophic ca bon demand in he mesopelagic no heas A lan ic, Geophys. Res. Le .,37, L09602, doi:10.1029/2010GL043105. 1. In oduc ion [2] I is gene ally accep ed ha he deep‐wa e he e o- ophic ood web elies on he o ganic ma e (OM) gene - a ed by p ima y p oduc ion in he sun‐li su ace wa e s. On a global a e age, abou 30% o he su ace wa e ’s p ima y p oduc ion is expo ed in o he da k ocean as sedimen ing pa icles [A ís egui e al., 2005b; Buessele and Boyd, 2009]. Al hough he concen a ion o dissol ed o ganic ca bon (DOC) is gene ally abou 10 imes highe han ha o pa icula e o ganic ca bon (POC), he su ace‐expo ed DOC pool makes i g ea es con ibu ion o oxygen con- sump ion in he uppe ocean [Hansell e al., 2009]) and i leas a g ea e dep hs (abou 10% o oxygen consump ion [A ís egui e al., 2002]). Hence, passi ely sinking pa icles o igina ing om he eupho ic zone ha e been conside ed as he p incipal sou ce o o ganic ca bon a ailable o he he e o ophic ood web in he ocean’s in e io [Buessele e al., 2007]. The majo i y o he POC expo ed om he eupho ic zone is emine alized in he mesopelagic laye (be ween 100–1000 m dep h), leading o a ypical exponen ial a enua ion o he sinking POC concen a ion wi h dep h. [3] Assuming mass balance, he supply a e o o ganic ca bon (gene ally calcula ed om sinking POC collec ed by sedimen aps) eaching he ocean’s in e io should ma ch he ca bon demand o he he e o ophic bio a inhabi ing he meso‐and ba hypelagic ealm. The deep‐wa e bio a is as ly domina ed by p oka yo es, in e ms o abundance and biomass. Howe e , he p oka yo ic o ganic ca bon demand ( he o al amoun o o ganic ca bon equi ed o sus ain he he e o ophic me abolism o p oka yo es, de e mined as espi a ion plus p oduc ion, PCD) has been shown o con- inuously exceed he sinking POC lux in o he da k ocean [Bu d e al., 2010]. Recen es ima es epo a misma ch be ween deep‐wa e PCD and sinking POC lux by up o 2– 3 o de s o magni ude [Rein hale e al., 2006; S einbe g e al., 2008; Bal a e al., 2009]. Mo eo e , a global budge ing exe cise indica ed ha e en he highes es ima e o sinking POC lux om su ace wa e s would only explain abou 50% o he measu ed oxygen consump ion in he da k ocean [del Gio gio and Dua e, 2002]. This pa adoxical imbalance has been shown o a y spa ially. PCD was 3–4 imes and a ound 10 imes g ea e han he sinking POC lux in he sub opical and suba c ic Paci ic, espec i ely [S einbe g e al., 2008]. This s ong imbalance be ween POC supply and demand ep esen s one o he g ea challenges in con- empo a y biological oceanog aphy and ma ine biogeo- chemis y, and indica es majo gaps in ou unde s anding o he deep ocean ca bon lux. I is appa en ha some majo componen s and aspec s o o ganic ca bon s ocks and luxes ha e no been aken in o accoun adequa ely. [4] One o he majo POC pools in he ocean’s in e io no adequa ely aken in o accoun in he oceanic ca bon budge s 1 Facul ad de Ciencias del Ma , Uni e sidad de Las Palmas de G an Cana ia, Las Palmas de G an Cana ia, Spain. 2 Facul y Cen e o Ecology, Depa men o Ma ine Biology, Uni e si y o Vienna, Vienna, Aus ia. 3 Depa amen de Biologia Ma ina i Oceanog a ia, Ins i u de Ciències del Ma , CSIC, Ba celona, Spain. 4 Depa men o Biological Oceanog aphy, Royal Ne he lands Ins i u e o Sea Resea ch, Den Bu g, Ne he lands. Copy igh 2010 by he Ame ican Geophysical Union. 0094‐8276/10/2010GL043105 GEOPHYSICAL RESEARCH LETTERS, VOL. 37, L09602, doi:10.1029/2010GL043105, 2010 L09602 1o 6 is slow‐sinking, o almos suspended non‐sinking POC (nsPOC) collec ed wi h oceanog aphic bo les bu , due o hei buoyan na u e, no accumula ing in sedimen aps used o de e mine sinking POC lux [A ís egui e al., 2009]. In a p e ious s udy, Bal a e al. [2009] ound a signi ican co ela ion be ween nsPOC and po en ial espi a ion ( he main pa ame e de e mining PCD) in he deep wa e s o he sub opical No heas A lan ic, suppo ing he iew ha nsPOC plays a key ole in da k ocean me abolism, and hence in supplying bioa ailable subs a es o suppo he PCD. Ne e heless, he quan i a i e o igin o his nsPOC s ill emains la gely enigma ic. The bulk meso‐and ba hy- pelagic nsPOC may come om di e en sou ces: i) om sel ‐assembly o dissol ed o ganic ma e ial yielding po ous mic ogels ha can be eadily colonized by mic oo ganisms [Chin e al., 1998], ii) om sinking pa icles disagg ega ed by physical o ces [Bu d and Jackson, 2009] o he ac i i y o mic obes and zooplank on [She idan e al., 2002], iii) om la e ally ad ec ed nsPOC, o i ) om in si u p oduc ion o o ganic ma e ial due o p oka yo ic chemoau o ophs. [5] He e we quan i y he con ibu ion o da k ocean chemosyn hesis o PCD in he sub opical No heas A lan ic and compa e i wi h he con ibu ion o he sinking POC lux. We use da a colla ed om he meso‐and ba hypelagic No h A lan ic on sedimen ing pa icula e o - ganic ma e (POM) lux, POM s anding s ock ( hus in- cluding he esiden nsPOC) and PCD o e‐e alua e he appa en disc epancy be ween p oka yo ic o ganic ma e demand and supply in he ocean’s in e io . 2. Me hods 2.1. S udy Si e and Sampling [6] Mo e han 9000 km we e co e ed du ing he AR- CHIMEDES‐I (No embe –Decembe 2005) c uise on boa d RV Pelagia o esol e he a eal a iabili y in o ganic ma e and p oka yo ic ac i i y in he meso‐and ba hypelagic wa e s o he eas e n No h A lan ic (Figu e S1 in Tex S1 o he auxilia y ma e ial). 1 Samples we e aken om se en dep hs: he su ace mixed laye (a e age dep h 50 m) o pa icula e o ganic ma e (POM) and elec on anspo sys em (ETS) only, he base o he mixed laye (100 m laye ), he mesopelagic (250, 500 and 900 m), he No h Eas A lan ic Deep Wa e (NEADW; a e age dep h 2750 m) and he Lowe Deep Wa e (LDW; a e age dep h 4000 m). Samples om he dis inc wa e masses we e collec ed wi h 12 L NOEX (no oxygen exchange) bo les moun ed on a CTD (conduc i i y, empe a u e, dep h) ame o de e mine o al p oka yo ic abundance, leucine inco po a ion, POM, ETS and da k DIC ixa ion as desc ibed below. 2.2. P oka yo ic Abundance, He e o ophic Me abolism and Pa icula e O ganic Ma e Concen a ions [7] P oka yo ic abundance, leucine inco po a ion, pa ic- ula e o ganic ca bon and ni ogen, espi a o y ac i i y o he elec on anspo sys em (ETS) and non‐sinking pa icula e o ganic ca bon (nsPOC) and ni ogen (nsPON) we e ana- lyzed as explained in a p e ious s udy [Bal a e al., 2009] (see also auxilia y ma e ial). 2.3. Dissol ed Ino ganic Ca bon (DIC) Fixa ion [8] DIC ixa ion was measu ed ia he inco po a ion o [ 14 C]‐bica bona e (3.7 × 10 6 Bq, Ame sham) in 50 ml seawa e samples. T iplica e samples and o maldehyde‐ ixed blanks we e incuba ed in he da k a in si u empe a- u es o 60–72 h. Incuba ions we e e mina ed by he addi ion o o maldehyde (2% inal concen a ion) o he samples, il a ion on o 0.2‐mm polyca bona e il e s and insing wi h 10 ml o ul a‐ il e ed seawa e (<30 kDa). A e wa d, he il e s we e exposed o a ume o concen- a ed HCl o 12 h, ans e ed in o scin illa ion ials and a e adding 8 ml scin illa ion cock ail (Canbe a‐Packa d, Fil e Coun ), coun ed in he scin illa ion coun e o 10 min. The esul ing mean disin eg a ions pe minu e (DPM) o he samples we e co ec ed o he mean DPM o he blanks and con e ed in o DIC ixed o e ime and co ec ed o he na u al DIC concen a ions as measu ed by con inuous low analysis [S oll e al., 2001]. 3. Resul s and Discussion [9] Unlike he gene al exponen ial decline in sinking POC wi h dep h [Ma in e al., 1987], he a e age concen a ions o nsPOC and nsPON emained ai ly cons an wi h dep h down o ba hypelagic wa e s (4000 m dep h) o he (sub) opical No heas A lan ic (Figu es 1a and 1b). This pa e n con as s wi h he epo ed dec ease wi h dep h o nsPOC a he Be muda A lan ic Time‐se ies (BATS) s a ion, in he cen e o he No h A lan ic sub opical Gy e, bu is simila o he dis ibu ion obse ed by Alonso‐González e al. [2009] in he Cana y Cu en (CanC), a he no heas e n side o ou sampling egion. O e all, ou nsPOC alues spans he ange o he obse ed CanC and BATS con- cen a ions (Figu e S2 in Tex S1 o he auxilia y ma e ial), sugges ing a ansi ional con inen al shel ‐open ocean g a- dien in nsPOM concen a ions. Gene ally, he p oka yo ic con ibu ion o he nsPOC and nsPON dec eased wi h dep h (Figu es 1c and 1d). Sub ac ing he p oka yo ic con ibu- ion om he bulk nsPOC and nsPON pool, we ob ain he amoun po en ially a ailable o he e o ophic u iliza ion o nsPOC (nsPOC_A ) and nsPON (nsPON_A ), which did no exhibi a gene al dep h‐ ela ed end (Figu es 1e and 1 ). The a io nsPOC_A : nsPON_A was also ai ly cons an h oughou he wa e column sugges ing ha he e a e no majo shi s in he C:N a io o nsPOM in deep‐wa e s (Figu e 1g), in con as o he epo ed inc easing C:N a ios wi h dep h o sedimen ing POM and DOM [Schneide e al., 2003; Hopkinson and Vallino, 2005]. This s abili y in he elemen al composi ion o suspended POM, in combina ion wi h i s ai ly cons an concen a ion h oughou he wa e column o ou egion o s udy sugges s ha i is ei he no u ilized bio ically o ha i s u iliza ion by he deep‐sea bio a is ma ched by in si u p oduc ion o ex e nal impo o nsPOM. Alonso‐González e al. [2009] obse ed lowe a - e age C:N a ios in he CanC han in ou s udy, al hough hei a ios clea ly inc eased in hei wes e n s a ions o he sampling box, acco ding o he measu ed high espi a ion o nsPOC h ough i s wes wa d anspo . [10] P oka yo ic espi a ion (R) is he main pa ame e a ec ing he PCD in he deep A lan ic, as i is ypically 1– 1 Auxilia y ma e ials a e a ailable in he HTML. doi:10.1029/ 2010GL043105. BALTAR ET AL.: DARK CO 2 FIXATION AND C DEMAND L09602L09602 2o 6 2 o de s o magni ude highe han p oka yo ic he e o ophic p oduc ion [Rein hale e al., 2006; Bal a e al., 2009]. The e o e, ou PCD es ima es g ea ly ely on he con e sion o measu emen s o he elec on anspo sys em (ETS) o R, i.e., he R:ETS a io used (see auxilia y ma e ial). Ou PCD es ima es we e b acke ed based on an R:ETS a io o 0.086, de i ed om bac e ial cul u es in senescen phase [Ch is ensen e al., 1980], and o 0.6, ob ained om he Figu e 1. Box‐Whiske plo o he e ical dis ibu ion o (a) bulk non‐sinking pa icula e o ganic ca bon (nsPOC) and (b) ni ogen (nsPON), con ibu ion o he p oka yo ic biomass o he bulk (c) nsPOC and (d) nsPON, po en ially a ailable (e) nsPOC and ( ) nsPON a e sub ac ing he p oka yo ic C‐and N‐biomass, espec i ely, and (g) he a io o po en ially a ailable nsPOC o nsPON. All o ganic ma e concen a ions a e in mmol l −1 . BALTAR ET AL.: DARK CO 2 FIXATION AND C DEMAND L09602L09602 3o 6 same cul u es in exponen ial g ow h phase [Ch is ensen e al., 1980] and in si u measu emen s o ac i e mesopelagic p oka yo es in he CanC egion [A ís egui e al., 2005a]. The PCD dec eased by one o de o magni ude om he base o he eupho ic zone owa ds he ba hypelagic zone independen o he R:ETS a io used (Table 1). The oxygen u iliza ion a es (OUR) epo ed o he cen e s o he No h and Sou h A lan ic sub opical Gy es [Jenkins, 1982; Jenkins and Wallace, 1992; B ea, 2008] a e wi hin he ange o ou PCD es ima es (Table 1). Assuming ha hese bio- geochemical es ima es ep esen a e age alues om ou egion o s udy, he R:ETS a io should be close o 0.2. Ne e heless, i is mo e plausible o assume ha he R:ETS a io a ies be ween 0.2 and 0.6, since ou egion o s udy spans a ansi ion zone wi h mo e nsPOM han obse ed in he cen e s o he sub opical Gy es. [11] Dissol ed ino ganic ca bon (DIC) ixa ion by che- moau o ophic mic obes occu s h oughou he deep wa e s o he A lan ic [He ndl e al., 2005], amoun ing on a e age 12 ± 5 mmol C m −3 d −1 in he mesopelagic ealm o he (sub) opical No heas A lan ic (Table 1). This eshly p oduced o ganic ca bon ep esen s an nsPOC sou ce in he meso‐ and ba hypelagic wa e s, as mic obial cells a e oo small o sedimen . The au och honously p oduced nsPOC po en ially accoun s o 72 ± 53% o 12 ± 9% (conside ing an R:ETS o 0.086 and 0.6, espec i ely) o he daily he e o ophic p o- ka yo ic ca bon demand in he mesopelagic ealm (Table 2). [12] Fo compa ison, he sinking POC lux based upon a model om a compila ion o sedimen ap da a o he No h A lan ic [An ia e al., 2001] was used o es ima e he po- en ial con ibu ion o he sinking POC o PCD. We calcu- la ed he sinking POC using he su ace p ima y p oduc ion (PP) es ima es om he NE A lan ic gy e [Longhu s e al., 1995] (28 mmol C m −2 d −1 ), om he wes e n gy e [S einbe g e al., 2001] (35 mmol C m −2 d −1 ) and as an uppe limi 50 mmol C m −2 d −1 ( o he en i e No h A lan ic [Longhu s e al., 1995] including empe a e egions whe e PP is highe ). The po en ial con ibu ion o he sinking POC amoun s o 4–6% o he PCD pe day when using a su ace PP o 28 and 35 mmol C m −2 d −1 , espec i ely (Table 2). Only when using he un ealis ically high su ace PP o 50 mmol C m −2 d −1 o his (sub) opical mid‐oceanic egion, he con ibu ion o he sinking POC o he mesopelagic PCD equals he con ibu ion (12%) o he da k CO 2 ixa ion (Table 2). Despi e he a he low DIC ixa ion a es in he ba hypelagic ealm, e en in his laye he con ibu ion o he sinking POC o he PCD does no exceed he con ibu ion de i ed om DIC ixa ion (Table 2). Thus, a signi ican ac ion (a leas simila o he sinking POC con ibu ion) o he o ganic ca bon equi ed by he meso‐and ba hypelagic mic obial communi y could be supplied by chemoau o o- phic CO 2 ixa ion in he (sub) opical No heas A lan ic’s in e io . [13] As shown p e iously, he majo ene gy sou ce o p oka yo ic DIC ixa ion is likely de i ed om ammonia oxida ion by C ena chaeo a, as a chaeal amoA genes a e by a mo e abundan han bac e ial amoA genes in he meso- pelagic ealm o he No h A lan ic [Agogué e al., 2008]. Table 1. Compa ison o he Va ia ion in he Di e en Dep h Laye s o he P oka yo ic Ca bon Demand a Dep h (m) PCD (R:ETS = 0.086) PCD (R:ETS = 0.6) OUR NA l OUR SA l AP 100 58.9 353.4 41.3 250 18.3 109.5 36.5 26.4 32.4 500 11.9 71.5 14.7 16.8 3.7 900 4.2 25.2 6.5 12.3 0.3 2750 3.3 19.9 0.2 4000 4.7 28.5 0.3 a PCD, p oka yo ic ca bon demand. Assuming an R:ETS a io o 0.086 and 0.6, oxygen u iliza ion a es (OUR) epo ed o he No h A lan ic Sub opical Gy e (OUR NA l) [Jenkins, 1982], and o he Sou h A lan- ic Sub opical Gy e (OUR SA l) [B ea, 2008], and da k DIC ixa ion a es (AP, au o ophic p oduc ion). Me abolic a es in mmol C m −3 d −1 . Table 2. Po en ial Con ibu ion (in %) o Da k CO 2 Fixa ion (AP) and o he A ailable Sinking POC o he PCD a Dep h AP Sinking POC (PP = 28) Sinking POC (PP = 35) Sinking POC (PP = 50) % Con ibu ion o PCD Assuming R:ETS =0.086 100 70 55 82 154 250 177 38 57 106 500 31 18 27 51 900 7 19 29 54 2750 5 4 6 10 4000 7 1 2 4 mesop a g 72 ± 53 25 ± 6 37 ± 10 70 ± 18 ba hy a g 6 ± 1 3 ± 1 4 ± 2 7 ± 3 Mesop AP: Sinking a io 2.8 1.9 1.0 Ba hyp AP: Sinking a io 2.4 1.6 0.9 % Con ibu ion o PCD Assuming R:ETS =0.6 100 12 9 14 26 250 30 6 9 18 500 5 3 5 8 900 1 3 5 9 2750 1 1 1 2 4000 1 0 0 1 mesop a g 12 ± 9 4 ± 1 6 ± 1 12 ± 3 ba hy a g 1 0 1 1 Mesop AP: Sinking a io 2.8 1.9 1.0 Ba hyp AP: Sinking a io 2.4 1.6 0.9 a Assuming an R:ETS o 0.086 and 0.6. The con ibu ion om he sinking POC was in e ed om a POC lux model [An ia e al., 2001] assuming a su ace p ima y p oduc ion (PP) o 28 mmol C m −2 d −1 (NE A lan ic gy e [Longhu s e al., 1995]), 35 mmol C m −2 d −1 (wes e n gy e [S einbe g e al., 2001]) and o 50 mmol C m −2 d −1 (N A lan ic [Longhu s e al., 1995]). BALTAR ET AL.: DARK CO 2 FIXATION AND C DEMAND L09602L09602 4o 6 Based on he adioca bon signa u e o a chaeal lipids, i has been shown ecen ly ha 83% o he a chaeal ca bon is de i ed by au o ophy in he sub opical mesopelagic No h Paci ic (a 670 m dep h) [Ingalls e al., 2006]. The adio- ca bon signa u e o DNA collec ed om mesopelagic Pa- ci ic wa e s (670–915 m) allowed o di e en ia e be ween he h ee majo ca bon pools ha a e po en ially a ailable o p oka yo es: esh DOC eleased om POC (D 14 C> +50‰), ambien DIC (D 14 C∼−200 o −100 ‰), and aged bulk DOC (D 14 C=−525‰)[Hansman e al., 2009]. These au ho s concluded ha bo h DIC and esh DOC (p esum- ably eleased om sinking POC) a e u ilized subs an ially, while ambien DOC is no a majo subs a e o mesopelagic p oka yo es [Hansman e al., 2009]. The e is also e idence o conside able chemoli ho ophic p oduc ion on sinking POC collec ed by sedimen aps deployed in he mesope- lagic (100–750 m dep h) No h Paci ic, whe e p oka yo es con ibu es be ween 7–90% o he o al mic obial p oduc- ion [Ka l e al., 1984]. [14] Taken oge he , he cu en pe cep ion on he de- pendence o he da k ocean’s he e o ophic mic obial ac- i i y on sedimen ing POC, and he p e iously epo ed misma ch be ween o ganic ca bon supply and demand need e ision [Rein hale e al., 2006; S einbe g e al., 2008; Bal a e al., 2009; Bu d e al., 2010]. The la ge and ai ly cons an s ock o buoyan , nsPOC needs o be conside ed as a po en ially a ailable dynamic pool o POC o he e o o- phic deep‐wa e mic obes. We ha e shown ha abou 12 ± 9–72 ± 53% o he amoun o PCD equi ed by mic o- he e o ophs in he mesopelagic ocean is po en ially sup- plied by deep‐wa e chemoli ho ophs ia DIC ixa ion. The e o e, he appa en gap be ween he e o ophic o ganic ma e demand and supply in he mesopelagic ealm migh be subs an ially smalle han p e iously hough . Ne e he- less, he ex e nal sou ces o his nsPOM s ill needs o be cons ained. Figu e S3 (in Tex S1 o he auxilia y ma e ial) illus a es he o e all con ibu ion o au o ophic p oduc ion (AP) and sinking POC o PCD assuming a PP o 28 mmol C m −2 d −1 and a R:ETS ange o 0.4–0.2, which based on he abo e in o ma ion p obably ep esen s ealis ic a e age alues o ou egion o s udy. The iew eme ging om Figu e S3 is ha , in spi e o he signi ican con ibu ion o AP o PCD a conside able ac ion o he PCD s ill needs o be accoun ed by o he sou ces. Acco ding o ou obse a- ions, we sugges ha con inuous la e al ad ec ion o nsPOM om he con inen al ma gins may ep esen an impo an ac ion o he missing ca bon espi ed in ou egion o s udy. Fu u e esea ch should ocus on e ining he nu i i e quali y o buoyan nsPOC e sus sedimen ing POC. The e ined pa hways o o ganic ma e supply and demand in he da k ocean migh allow us o a i e a a mechanis ic unde s anding o deep ocean ood web s uc u e and ac i i y and ul ima ely, should lead o imp o ed models on he da k ocean’s ole in global ca bon cycling. [15]Acknowledgmen s. We hank he cap ain and c ew o R/V Pelagia o hei help du ing wo k a sea. A. Smi pe o med he leucine inco po a- ion measu emen s. M. F. Mon e o, and M. Espino helped wi h he Elec on T anspo Sys em analyses and I. J. Alonso‐González wi h he pa icula e o ganic ma e measu emen s. Wa e masses we e iden i ied by H. M. an Aken. This esea ch was suppo ed by a p edoc o al Fellowship o he Spanish Minis y o Educa ion and Science (AP2005‐3932) o F.B., a g an o he Ea h and Li e Science Di ision o he Du ch Science Founda- ion (ALW‐NWO; ARCHIMEDES p ojec , 835.20.023) o G.J.H. and a g an o he Spanish Minis y o Educa ion and Science o J. A. (Remolinos Oceánicos y Deposiciones A mos é icas (RODA) p ojec ; CTM 2004‐ 06842‐C03/MAR). The wo k was ca ied ou wi hin he ame o he EU ‘Ne wo ks o Excellence’Ma Be and Eu Oceans. Re e ences Agogué, H., M. B ink, J. Dinasque , and G. J. He ndl (2008), Majo g adi- en s in pu a i ely ni i ying and non‐ni i ying A chaea in he deep No h A lan ic, Na u e,456, 788–791, doi:10.1038/na u e07535. Alonso‐González, I., J. A ís egui, J. C. Vilas, and A. He nández‐Gue a (2009), Suspended POC anspo and consump ion in su ace and deep wa e s o he Cana y Cu en egion: A box model s udy, Global Biogeo- chem. Cycles,23, GB2007, doi:10.1029/2008GB003185. An ia, A. N., e al. (2001), Basin‐wide pa icula e ca bon lux in he A lan- ic Ocean: Regional expo pa e ns and po en ial o a mosphe ic CO 2 seques a ion, Global Biogeochem. Cycles,15, 845–862, doi:10.1029/ 2000GB001376. A ís egui, J., C. M. Dua e, S. Agus i, M. Do al, X. A. Al a ez‐Sagado, and D. A. Hansell (2002), Dissol ed o ganic ca bon suppo o espi a- ion in he da k ocean, Science,298, 1967, doi:10.1126/science.1076746. A ís egui, J., C. M. Dua e, J. M. Gasol, and L. Alonso‐Sáez (2005a), Ac- i e mesopelagic p oka yo es suppo high espi a ion in he sub opical no heas A lan ic Ocean, Geophys. Res. Le .,32, L03608, doi:10.1029/ 2004GL021863. A ís egui, J., S. Agus í, J. J. Middelbu g, and C. M. Dua e (2005b), Respi a ion in he mesopelagic and ba hypelagic zones o he ocean, in Respi a ion in Aqua ic Ecosys ems,edi edbyP.A.delGio gioand P. J. L. B. Williams, pp. 181–205, Ox o d Uni . P ess, Ox o d, U. K. A ís egui, J., J. M. Gasol, C. M. Dua e, and G. J. He ndl (2009), Mic obial oceanog aphy o he da k ocean’s pelagic ealm, Limnol. Oceanog ., 54(5), 1501–1529. Bal a , F., J. A ís egui, J. M. Gasol, E. Sin es, and G. J. He ndl (2009), E idence o p oka yo ic me abolism on suspended pa icula e o ganic ma e in he da k wa e s o he sub opical No h A lan ic, Limnol. Oceanog .,54(1), 182–193. B ea, S. (2008), Ci culación, mezcla, en ilación y mine alización de las aguas del A lán ico Su , Ph.D. hesis, Uni . o Vigo, Vigo, Spain. Buessele , K. O., and P. W. Boyd (2009), Shedding ligh on p ocesses ha con ol pa icle expo and lux a enua ion in he wiligh zone o he open ocean, Limnol. Oceanog .,54(4), 1210–1232. Buessele , K. O., e al. (2007), Re isi ing ca bon lux h ough he ocean’s wiligh zone, Science,316, 567–570, doi:10.1126/science.1137959. Bu d, A. B., and G. A. Jackson (2009), Pa icle agg ega ion, Annu. Re . Ma . Sci.,1,65–90. Bu d, A. B., e al. (2010), Assesing he appa en imbalance be ween geo- chemical and biochemical indica o s o meso‐and ba hypelagic biolog- ical ac i i y: Wha he @$#! is w ong wi h he p esen calcula ions o ca bon budge ?, Deep Sea Res., Pa II, in p ess. Chin, W‐L., M. V. O ellana, and P. Ve dugo (1998), Spon aneous assem- bly o ma ine dissol ed o ganic ma e in o polyme gels, Na u e,391, 568–572. Ch is ensen, J. P., T. G. Owens, A. H. De ol, and T. T. Packa d (1980), Respi a ion and physiological s a e in ma ine bac e ia, Ma . Biol. Be lin, 55, 267–276, doi:10.1007/BF00393779. del Gio gio, P. A., and C. M. Dua e (2002), Respi a ion in he open ocean, Na u e,420, 379–384, doi:10.1038/na u e01165. Hansell, D. A., C. A. Ca lson, D. J. Repe a, and R. Schli ze (2009), Dissol ed o ganic ma e in he ocean, Oceanog aphy,22(4), 202–211. Hansman, R. L., S. G i in, J. T. Wa son, E. R. M. D u el, and A. E. Ingalls (2009), The adioca bon signa u e o mic oo ganisms in he mesopelagic ocean, P oc. Na l. Acad. Sci. U. S. A.,106(16), 6513–6518, doi:10.1073/ pnas.0810871106. He ndl, G. J., T. Rein hale , E. Tei a, H. . Aken, C. Ve h, A. Pe n hale , and J. Pe n hale (2005), Con ibu ion o A chaea o o al p oka yo ic p oduc ion in he deep A lan ic Ocean, Appl. En i on. Mic obiol.,71, 2303–2309, doi:10.1128/AEM.71.5.2303-2309.2005. Hopkinson, C. S., J ., and J. J. Vallino (2005), E icien expo o ca bon o he deep ocean h ough dissol ed o ganic ma e , Na u e,433, 142–145, doi:10.1038/na u e03191. Ingalls, A. E., S. R. Shah, R. L. Hansman, L. I. Aluwiha e, G. M. San os, E. R. M. D u el, and A. Pea son (2006), Quan i ying a chaeal communi y au o ophy in he mesopelagic ocean using na u al adioca bon, P oc. Na l. Acad. Sci. U. S. A.,103, 6442–6447, doi:10.1073/pnas.0510157103. Jenkins, W. J. (1982), Oxygen u iliza ion a es in he No h A lan ic Sub- opical Gy e and p ima y p oduc ion in oligo ophic sys ems, Na u e, 300, 246–248, doi:10.1038/300246a0. Jenkins, W. J., and D. W. R. Wallace (1992), T ace Based In e ences o New P ima y P oduc ion in he Sea, pp. 299–316, Plenum, New Yo k. BALTAR ET AL.: DARK CO 2 FIXATION AND C DEMAND L09602L09602 5o 6 Ka l, D. M., G. A. Knaue , J. H. Ma in, and B. B. Wa d (1984), Bac e ial chemoli ho ophy in he ocean is associa ed wi h sinking pa icles, Na u e,309,54–56, doi:10.1038/309054a0. Longhu s , A., S. Sa hyend ana h, T. Pla , and C. Ca e hill (1995), An es ima e o global p ima y p oduc ion in he ocean om sa elli e adi- ome e da a, J. Plank on Res.,17,1245–1271, doi:10.1093/plank / 17.6.1245. Ma in, J. H., G. A. Knaue , D. M. Ka l, and W. W. B oenkow (1987), VERTEX: Ca bon cycling in he no heas Paci ic, Deep Sea Res., Pa A,34, 267–285, doi:10.1016/0198-0149(87)90086-0. Rein hale , T., H. . Aken, C. Ve h, P. J. l. Williams, J. A is egui, C. Robinson, P. Leba on, and G. J. He ndl (2006), P oka yo ic espi a ion and p oduc- ion in he meso‐and ba hypelagic ealm o he eas e n and wes e n No h A lan ic basin, Limnol. Oceanog .,51, 1262–1273. Schneide , B., R. Schli ze , G. Fische , and E. M. Nö hing (2003), Dep h‐ dependen elemen al composi ions o pa icula e o ganic ma e (POM) in he ocean, Global Biogeochem. Cycles,17(2), 1032, doi:10.1029/ 2002GB001871. She idan, C. C., C. Lee, S. G. Wakeham, and J. K. B. Bishop (2002), Suspended pa icle o ganic composi ion and cycling in su ace and midwa e s o he equa o ial Paci ic Ocean, Deep Sea Res., Pa I, 49, 1983–2008, doi:10.1016/S0967-0637(02)00118-8. S einbe g, D. K., C. A. Ca lson, N. R. Ba es, R. J. Johnson, A. F. Michaels, and A. H. Knap (2001), O e iew o he US JGOFS Be muda A lan ic Time‐se ies S udy (BATS): A decade‐scale look a ocean biology and biogeochemis y, Deep Sea Res., Pa II,48,1405–1447, doi:10.1016/ S0967-0645(00)00148-X. S einbe g, D. K., B. A. Van Mooy, K. Buessele , P. W. Boyd, T. Koba i, and D. M. Ka l (2008), Bac e ial s. zooplank on con ol o sinking pa icle lux in he ocean’s wiligh zone, Limnol. Oceanog .,53(4), 1327–1338. S oll, M. H. C., K. Bakke , G. H. Nobbe, and R. R. Haese (2001), Con inuous‐ low analysis o dissol ed ino ganic ca bon con en in seawa e , Anal. Chem.,73(17), 4111–4116, doi:10.1021/ac010303 . J. A ís egui and F. Bal a , Facul ad de Ciencias del Ma , Uni e sidad de Las Palmas de G an Cana ia, Campus Uni e si a io de Ta i a, E‐35017 Las Palmas de G an Cana ia, Spain. ([email p o ec ed]) J. M. Gasol, Depa amen de Biologia Ma ina i Oceanog a ia, Ins i u de Ciències del Ma , CSIC, Pg. Ma í im de la Ba celone a 37‐49, E‐08003 Ba celona, Spain. G. J. He ndl, Depa men o Biological Oceanog aphy, Royal Ne he lands Ins i u e o Sea Resea ch, NL‐1790 AB Den Bu g, Ne he lands. T. Rein hale and E. Sin es, Facul y Cen e o Ecology, Depa men o Ma ine Biology, Uni e si y o Vienna, Al hans . 14, A‐1090 Vienna, Aus ia. BALTAR ET AL.: DARK CO 2 FIXATION AND C DEMAND L09602L09602 6o 6