Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussions . Planktonic life 2 Biogeosciences 17038 17037 This discussion paper is/has been under review for the journal Biogeosciences (BG). Please refer to the corresponding final paper in BG if available. they supported large communitiesmal and vent, assemblages whale of fall, wood higher fall, organisms. and Hydrother- cold seep communities are able to make use of the the sun through theerotrophic consumers. process Until of the discovery photosynthesis,alternatives of either chemosynthesis to in as light 1887 primary byto energy Winogradsky, producers science. for Surprisingly, or the even het- productionwas after widely of the thought organic process to carbontion of be (Van remained chemosynthesis Dover, relatively 2000). unknown was insignificant With1977 observed, as the (Corliss it discovery a et of al., mechanism deep-sea 1979),not of hydrothermal it only primary vent became present systems clear produc- in that in the chemosynthetic microorganisms deep were sea where light energy from the sun is absent, but that in their entirety from terrestrial sources. 1 Introduction The Earth’s surface is dominated by organisms which depend on energy captured from indirectly provides oxygen, athetic byproduct microorganisms of require photosynthesis, tostages which synthesize of aerobic organic many chemosyn- carbon vent fromcally and CO produced cold organic seep matter invertebratesa as also large they portion directly disperse of feed to the onand new life photosyntheti- at vent so deep-sea and could chemosynthetic seep habitats notmicroorganisms systems. can survive While can be without linked persist to it, in thedeveloped a a sun its way small of absence. life portion These in of the small deep-sea anaerobically and which chemosynthetic involves exotic the organisms use of have resources originating Chemosynthetic communities in the deep-sea canseeps, be whale found at falls hydrothermal vents, and cold exist wood in falls. isolation While from thesedirectly solar communities energy, or much have indirectly of been on the suggested photosynthesis life to associated in with the them surface relies waters either of the oceans. The sun Abstract Biogeosciences Discuss., 9, 17037–17052, 2012 www.biogeosciences-discuss.net/9/17037/2012/ doi:10.5194/bgd-9-17037-2012 © Author(s) 2012. CC Attribution 3.0 License. Chemosynthesis in the deep-sea: life without the sun C. Smith Howarth and Smith, 523 West 6th St. SuiteReceived: 728 7 Los November Angeles, 2012 CA, – 90014 Accepted: USA 26Correspondence November to: 2012 C. – Smith Published: ([email protected]) 4 December 2012 Published by Copernicus Publications on behalf of the European Geosciences Union. 5 20 25 15 10 Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | cient means of ffi O provide the source of erence between the two 2 ff cient pathway than the Calvin and H ffi 2 17040 17039 ¨ auser, 1988) and on the prospects of life on other planets in erent electron donors and acceptors. While a wide range of electron ff ¨ achtersh into organic carbon compounds using the Calvin–Benson cycle (Van 2 into organic carbon compounds; the significant di 2 fixation, the reductive acetyl-CoA pathway is limited to anoxic environments, and and then undergoes reductive carboxylation to generate the pyruvate used in the 2 2 Depending on the nature of the electron acceptor in the reaction, chemosynthesis Like photosynthetic metabolism, chemosynthesis involves the conversion of inor- cycle for the generationthe of Wood–Ljungdahl ATP. Termed pathway, the after its reductivebe founders, acetyl-coenzyme used it A in requires pathway approximately the or (Berg one generation et ATP of to al., pyruvate 2010). whileCO During the the Calvin–Benson process, cyclefurther acetyl-CoA requires synthesis is seven of cellular formed material fromCO (Jannasch, 1985). two While molecules a more of indeed e anaerobic chemosynthetic microorganisms seemtion to in be deep-sea limited communities in to their locations distribu- that fit their anoxic needs, such as the hot munities (Jannasch, 1985; McCollomthat and make Shock, use 1997). of Likeversion aerobic plants, of chemosynthesis microorganisms CO couple theirDover, 2000). reduction On reaction the to otheranaerobic hand, the chemosynthesis some con- microorganisms have such developed as a the more Archaea that e use 1985). may either be aerobic orchemosynthesis anaerobic makes (Van use Dover, 2000). of As oxygenbic the as chemosynthesis name the relies suggests, primary on aerobic a electron variety acceptor,phur of while and acceptors sulphate. anaero- such Reduction as reactions nitrate, involvingenergy carbon oxygen than dioxide, tend sul- to those have using a larger alternativesis potential has electron the acceptors, potential and to so produce aerobic more chemosynthe- ATP and tends to dominate most deep-sea com- ganic CO is that in chemosynthesis,found the between di reduction reactionsdonors are are fueled suitable by for thesignificant use potential for by energy deep-sea chemosynthetic communities microorganisms are (see sulphide Fig. and 2), methane the (Jannasch most and Mottl, carbon and electrons respectively (see Fig. 1). 2 Discussions First observed in themicroorganisms deep sea are in able the toorganic 1970s, use chemosynthesis chemical sources. is energy Basic the to processchemosynthesis biochemistry generate and by organic photosynthesis, tells which are carbon comprised us from ofenergy that three in- source, fundamental all an elements: an electron metabolic donor,of and processes, photosynthesis, a including light carbon provides source the (Van Dover, energy 2000). while In CO the case from the influence ofremoved the from sun? the equation Could altogether? suchamine In the communities answering chemical these persist questions processes if wethe involved the must organisms in sun first and chemosynthesis ex- communities were as which to well rely be as on the it. structure of 1000 m where thegeomicrobiology last of of deep the sea sun’s hydrothermalthat light vents, it rays Jannasch was and can Mottl this stillthan (1985) be solar “dependence suggest energy” detected. of that In entirethetic made a communities ecosystems the in paper discovery the on on deep of geothermal sea the origins the so (terrestrial) vent of groundbreaking, systems prompting life rather new and (W theories otherour into own chemosyn- the solar system (Vanties Dover, thousands 2000). of meters But below is the it last rays true? of Do sunlight chemosynthetic really exist communi- in complete isolation otic relationships with chemosynthetic microorganisms andenvironment which are thus is able normally to characterized thriveet as in having al., an an 2006). extreme Much food of limitationsurface the (Rex waters, on energy which provided most by otherit photosynthetic deep-water can primary organisms make depend, production is its in exploited way the before into the depths, leaving only about 1–20 % to sink past a depth of chemical energy found in elements such as sulphide and methane because of symbi- 5 5 25 15 20 10 25 15 20 10 Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | erent vent ff ect the organisms ff 17042 17041 of tectonic plates during subduction or accretionary prisms. Or ff To the casual observer, it is easy to be lured into the view that hydrothermal vent Cold seep communities have been observed on active and passive margins of the In the case of hydrothermal vents and cold seeps, the search for life truly isolated To date, four distinct deep-sea habitats have been shown to provide the condi- and cold seep communities could persist in the absence of the sun. After all, they stores of methane (Sibuet and Olu,phide 1998). from While subterranean some cold reservoirsthe seeps (Paull actually action et release of sul- al., anaerobic sulphate-reducing 1984),ments. microorganisms The most sulphide working sites they in acquire release theother can it anoxic aerobic then chemosynthetic sedi- through microorganisms “seep” as out anThe of energy result the source of sediment (Van these Dover, and 2000). processes bea is used large a by amount deep- of seaganisms. environment primary rich productivity in through elements the suitable action for of chemosynthetic microor- (1998). In general thereright seems conditions to for be cold twovolcanoes seep basic and communities geological active to processes thrust form. thataccretions faults, They provide created can forced the by be o compression associatedthey forces with can within mud form sedimentary as erosion or landslides removes sediment from previously inaccessible 2007). These variations in chemicaland composition composition of of the the communities vent which fluid surround a the vent (Vancontinental Dover, shelves 2000). and rely on theslope. escape Active of margins methane are or associated sulphideone with from tectonic plate the activity continental under caused the byof the other, cold subduction while of seeps at tend passiveelements to that margins vary support no based them, subduction for on occurs. a local The full conditions sites review of and 24 the distinctive nature sites of see the Sibuet and escaping Olu neath the ridge and heatsthe up water significantly. Depending is on exposed to, the it pressureFig. may and also 3). temperature undergo The phase exact separation chemical intofields vapor composition and as of brine the the (see vent physical fluidquantities properties can of vary of brine, across vapor the di and rock hot change water from mix site as to they travel site up and towards the the various vent (Tivey, 2007). Once underground, the seawater flows over the hot magma chamber under- and anoxic, able to leach various metals and sulphur from the surrounding rock (Tivey, from the sun becomes morement interesting of tectonic as plates geological are phenomenaicals. responsible linked for Hydrothermal to the the vents release move- ofin are most both of areas volatile the where necessary gasesspreading chem- hot and centers metals, anoxic and exits hotspots seawater, theNew associated which with seabed. evidence can mid-ocean These published be ridges systemsits (Van in rich are Dover, journey 2008 2000). the by result bying. of traveling Tolstoy As et down the al. conduits water suggests in penetrates the that the crust vent ridge and water axis gradually begins heats, caused it by becomes tectonic slightly fractur- acidic teresting, these chemosynthetic communities havethat a whales clear and dependence trees on directlyproducers. the make As sun, use such, in the of, chemosynthetic orof communities are whale which themselves, carcasses rely photosynthetic and on primary sunken thesun. wood decomposition in the deep sea would cease to exist without the of large nutrient packages. Organiccasionally matter find from its the way productive into(Smith surface the et waters depths can al., in oc- 1989). thea Much lifetime form feasts of of are whale the quickly consumed carcasses easily(Collins by or large accessible et scavenging sunken organic al., fish, wood such nutrients 2005). aset in However, sleeper al., anaerobic sharks these 1997) breakdown and once of wood in (Duperronproduce whale et sulphide. bone al., The 2008; lipids decomposition Gaudron of (Demming et suchchemical al., materials energy 2010) can has for last been sulphide-reducing for shown chemoautotrophs decades, to providing (Van Dover, 2000). While in- 1985). tions and resources necessary todrothermal support vents, significant cold chemosynthetic seeps, communities: whale hy- nities falls on and whale wood and wood falls. falls The are chemosynthetic opportunistic, commu- capitalizing on the random appearance plumes of hydrothermal vents and the subsurface sediments of cold seeps (Jannasch, 5 5 25 15 20 10 25 15 20 10 Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Bathymodiolus thermophilus and erent animal phyla (Dubilier et al., ff 17044 17043 Rimicaris exoculata While the adult stages of many invertebrates at vents and cold seeps rely on Further links to photosynthesis in deep-sea communities can be found in the life- Given what we know aboutcesses the involved in community sustaining structure, deep-sea chemosynthetic biochemistry communities, and is it geological correct pro- to say or cold seep dothem they during begin their to adult stages acquireof (Adams the these et chemosynthetic al., invertebrates 2012). symbionts further Evidenceof that rely also whale will on suggests and that photosynthetically sustain wood many falls derived whichof resources play newly in a formed critical the vent role form and as seep stepping systems stones for (Distel the et colonization al., 2000). 3 Conclusions swimming and must forage for foodand in seep the plankton. invertebrates As such thejoin as planktotrophic larvae the of rest vent of theents marine that plankton derive they directly can(Van from Dover, only photosynthetic 2000). survive primary It by is production consuming only in organic once the nutri- these surface larval waters stages locate and settle on a new vent is so successful that2008). it occurs in at least seven di chemosynthetic symbionts, the lifetonic history larval of some stages of whichmaternal these investment, do organisms larval not involve stages plank- (Adams candevelopment. undergo et Both direct, al., direct lecithotrophic 2012). or anddependency planktotrophic Depending lecithotrophic on on development stored yolk are the for characterized amount nutrition, by of while larval planktotrophic larvae are primarily free- the case of vestimentiferan tubewormsIn and essence, vesicomyid host bivalves (Dubilier invertebrates et arestream al., of able the 2008). to necessary provide elements, such agen, as stable and carbon environment dioxide, in sulphide, with methane return a andFig. receive oxy- steady 4). organic The carbon relationship between from chemoautotrophic their microorganisms symbiotic and chemoautotrophs invertebrates (see shrimp or by simply having a long enough body to traverse the chemical gradient, as in easily accomplish this task, either by being more motile as in the case of alvinocarid lationships with many invertebrate hostcrobial species chemoautotrophs (Van and Dover, their 2000).tages host By in invertebrates pairing gain habitats up, tremendous such mi- temporal fitness as boundary advan- between cold life seeps and deathchemoautotrophic and can microbe hydrothermal be at quite vents, a narrow. hydrothermal where Ason vent, a the the life free spatial is fine living a aerobic line and constantoxygenated between struggle seawater, the providing to anoxic a remain vent vital fluid,ficult electron given providing acceptor. the The sulphide fact task or that is it methane,quickly exceptionally is as and dif- almost this the boundary impossible for changes organisms with of the currents. such Invertebrate small host size species to can move more (Boyle et al., 1985). history of many ofThese the communities metazoan are inhabitantschemoautotrophic microorganisms of able have hydrothermal developed extremely to vents productive and symbiotic flourish re- cold primarily seeps. because, in the deep, aerobic the presence of freeearth, oxygen both as in an the atmosphere electronprocess and acceptor. oceans, of Free because photosynthesis oxygen it (Van is isrequirement, released Dover, only as 2000). the present a Boyle notion byproduct on et that of“geothermal the al. these (terrestrial) deep argue rather sea that than chemosynthetic becauseleading. solar communities of While energy” depend one this (Jannasch could on argue and about“source” Mottl, the in 1985), technicalities biochemical of is reactions, what it mis- is isnot defined certainly as exist true the as these energy deep-sea they communities are could now in the absence of free oxygen produced by photosynthesis geothermal processes far removedever, from the sun’s the influence influence onan of these energy direct deep-sea “source”, solar communities the radiation.indirect comes role provider How- not of it as a plays a keysis. in element provider As photosynthetic for of pointed the out primary reduction by production, reactions Boyle et of but al. aerobic as (1985), chemosynthe- an a critical piece of aerobic chemosynthesis is make use of the chemical energy obtained from compounds that are produced by 5 5 25 20 10 15 25 15 20 10 Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | e, ff ¨ ugler, M., Alber, B. E., ect of restructuring the gen- ff , 1985. energy obtained through geothermal and ff 17046 17045 erential response in scavenging and non-scavenging demersal ff doi:10.1126/science.230.4725.496-d Green, K., Williams, D., Bainbridge,springs A., on Crane, the K., Galapagos and Rift, van Science, Andel, 203, T. 1073–1083, H.: 1979. Submarinebasis thermal of a chemoautotrophicbone-colonizing invertebrate bacteria community and at invertebrate170, a 1997. endosymbionts, whale Miscrosc. fall Res. on Tech., the 37, deep 162– seafloor: environmental gradient: a di deep-sea fish, P. Roy. Soc. B-Biol. Sci., 272, 2051–2057, 2005. ence, 230, 4725, and Fuchs, G.:2010. Autotrophic carbon fixation in archaea, Nat. Rev. Microbiol., 8, 447–460, Oceanography, 25, 256–268, 2012. The discovery of chemosynthetic communities in the deep sea, starting with hy- Corliss, J. B., Dymond, J., Gordon, L. I., Edmond,Deming, J. J. M., W., Reysenbach, von A. Herzen, L., R. Macko, S. P., A., Ballard, and R. Smith, D., C. R.: Evidence for the microbial Collins, M. A., Bailey, D. M., Ruxton, G. D., and Priede, I. G.: Trends in body size across an Boyle, E., Pirie, N. W., Jannasch, H. W., and Holger, W.: Ecosystems of deep-sea vents, Sci- Berg, I. A., Kockelkorn, D., Ramos-Vera, W. H., Say, R. F., Zarzycki, J., H Adams, D. K., Arellano, S. M., and Govenar, B.: Larval dispersal: vent life in the water column, not require the sundeep at sea make these use sites, ofoxygen remains requirements anaerobic as true. chemosynthesis the which A aerobic does version. smallvanish Even not without portion as have the the the of majority sun, same of organisms theremicroorganisms free life in exists to on the persist earth the deep would continued down potential in for the a perpetual small darkness group of of our lonely deepestReferences seas. microorganisms form tight symbiotic relationshipsability in for the non-photosynthetic deep primary and production have toet highlighted support al., the large 2000). communities While (Dubilier oftenof characterized the as life communities on in hydrothermal isolation vents,not from cold exist the seeps, in whale sun, its and much absence. wood The falls could underlying not point and however, that would there exists life which does activity for the last 30 yr (Van Dover, 2000). Invertebrate hosts and chemosynthetic eral view on the importance of the sun and has been an area of significant research plishes that feat. Although thesenot small have the and same seemingly impact insignificantfundamental in microorganisms the purpose do deep as as reminders their ofmore aerobic the alien counterparts, incredible to they adaptability us serve than of aters organisms more life. below What surviving the could surface in of be annot the anoxic solar ocean, environment processes. living thousands o of me- drothermal vents in 1977biological (Corliss discoveries et of al., the late 1979), 20th is century. possibly It one had the of e the most significant fact it is not thetotrophs only obtain chemosynthetic both lifestyle found their atsevering electron such the acceptors sites. last and Anaerobic link chemoau- donors to1985). from solar What geothermal energy processes, is that their“how truly aerobic much” significant cousins life could about lives not in deep-sea (Boyle isolation et chemosynthetic from al., communities the is sun, not but the fact that any life at all accom- requirement (Van Dover, 2000).thetic Furthermore, sites invertebrates vary atwood in falls deep-sea their either chemosyn- as direct directothers reliance providers survive on of on nutrients photosynthesis, the or productsvae some as (Adams of dispersal require et photosynthetic stepping al., primary whale stones, 2012). productionmunities while and However, as would even planktonic die though lar- the out vast withoutdiscovery majority the of of sun, these life I in communities believein these remains that com- the the intact. more deep-sea To significant focus is result on predictable, of aerobic the given chemosynthesis how dominant the process is, but ignores the ties have often been characterized1992), in the the notion literature is as only “lifeable partially without biomass true associated the and with sun” deep-sea can (Tunnicli seeps, communities be whale such misleading. as falls Almost hydrothermal and all vents, wood of cold ganisms falls the which depends observ- could on not the survive action in of complete aerobic isolation chemosynthetic from or- the sun due to their oxygen they depend solely on geothermal rather than solar energy? 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W.: Review Lecture: the chemosynthetic support of life and the microbial diversity Gaudron, S. M., Pradillon, F., Pailleret, M., Duperron S., Le Bris, N., and Gaill F.: Coloniza- Duperron, S., Laurent, M. C. Z., Gaill, F., and Gros, O.: Sulpher-oxidizing extracellular bacteria Dubilier, N., Bergin, C., and Lott, C.: Symbiotic diversity in marine animals: the art of harnessing Distel, D. L., Baco, A. R., Chuang, E., Morrill, W., Cavanaugh, C., and Smith, C. R.: Marine 5 5 30 25 10 20 15 10 Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | 17050 17049 List of potential electron donors and acceptors for chemosynthesis in the deep sea. Simplified equation for photosynthesis. Adapted from Takai et al. (2006). Fig. 2. Fig. 1. Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | . The host pro- Riftia pachyptila 17052 17051 to it via the blood. In return the symbiont generates organic carbon 2 and CO 2 Schematic drawing of a generic ridge vent system, showing the path seawater takes Schematic diagram of chemosynthetic symbiosis inside through aerobic chemosynthesis coupled(2012). to the Calvin–Benson cycle. Adapted from Rogers Fig. 4. vides a special tissueports of sulfide, the O trophosome for the chemoautotropic microorganisms and trans- Fig. 3. and the chemical processesTivey involved (2007). in modifying the composition of vent fluid. Adapted from