Abstract
Microbes possess a great genetic repertoire and metabolic versatility that allow them to face the extreme conditions of the deep sea, drive the biogeochemical cycles, and feed chemosynthetic web chains. These microbes respond to historical, global, regional, and local processes in deep-sea habitats and are influenced by microenvironmental variations and the availability of nutrients and electron acceptors to move and survive. By the use of a suite of different methods, as omics techniques and in situ measurements, buoyant particles and the light-independent chemoautotrophic microbes are increasingly being considered as important carbon sources to heterotrophic biota below the euphotic zone. Studies conducted in asphalt seeps, gas hydrates, sunken organic substrates, natural whale carcasses, and seamounts in the Southwestern Atlantic Ocean have revealed a largely unknown diversity of microbes and their high potential for biotechnology. Further promising discoveries are about to come with increasing efforts to determine the microbial community composition, their metabolic diversity, and ecological role in the deep ocean across oceanographic features.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Acinas SG, Sánchez P, Salazar G et al (2019) Metabolic architecture of the deep ocean microbiome. bioRxiv 635680. https://doi.org/10.1101/635680
Akerman NH, Butterfield DA, Huber JA (2013) Phylogenetic diversity and functional gene patterns of sulfur-oxidizing subseafloor Epsilonproteobacteria in diffuse hydrothermal vent fluids. Front Microbiol 4:185. https://doi.org/10.3389/fmicb.2013.00185
Alves Junior N, Meirelles PM, De Oliveira SE et al (2015) Microbial community diversity and physical–chemical features of the Southwestern Atlantic Ocean. Arch Microbiol 197:165–179. https://doi.org/10.1007/s00203-014-1035-6
Anantharaman K, Breier JA, Sheik CS et al (2013) Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria. Proc Natl Acad Sci U S A 110:330–335. https://doi.org/10.1073/pnas.1215340110
Arístegui J, Gasol JM, Duarte CM et al (2009) Microbial oceanography of the dark ocean’s pelagic realm. Limnol Oceanogr 54:1501–1529. https://doi.org/10.4319/lo.2009.54.5.1501
Baltar F, Arístegui J, Gasol JM et al (2010) Mesoscale eddies: hotspots of prokaryotic activity and differential community structure in the ocean. ISME J 8:1–14. https://doi.org/10.1038/ismej.2010.33
Baltar F, Lundin D, Palovaara J et al (2016) Prokaryotic responses to ammonium and organic carbon reveal alternative CO2 fixation pathways and importance of alkaline phosphatase in the mesopelagic North Atlantic. Front Microbiol 7:1670. https://doi.org/10.3389/fmicb.2016.01670
Benner R (2002) Chemical composition and reactivity. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Science, New York, pp 59–90
Bernardino AF, Smith CR, Baco AR et al (2010) Macrofaunal succession in sediments around kelp and wood falls in the deep NE Pacific and community overlap with other reducing habitats. Deep-Sea Res I 57:708–723
Bernardino AF, Levin LA, Thurber AR et al (2012) Comparative composition, diversity and trophic ecology of sediment macrofauna at vents, seeps and organic falls. PLoS One 7(4):e33515. https://doi.org/10.1371/journal.pone.0033515
Bienhold C, Zinger L, Boetius A et al (2016) Diversity and biogeography of bathyal and abyssal seafloor bacteria. PLoS One 11:e0148016
Bolhuis H, Cretoiu MS (2016) What is so special about marine microorganisms? Introduction to the Marine Microbiome—from diversity to biotechnological potential. In: Stal LJ, Cretoiu MS (eds) Marine Microbiome: an untapped source of biodiversity and biotechnological potential. Springer. https://doi.org/10.1007/978-3-319-33000-6
Canfield DE, Stewart FJ, Thamdrup B et al (2010) A cryptic cycle in oxygen-minimum-zone waters off the Chilean coast. Science 330:1375–1378. https://doi.org/10.1126/science.1196889
Case DH, Pasulka AL, Marlow JJ et al (2015) Methane seep carbonates host distinct, diverse, and dynamic microbial assemblages. mBio 6(6):e01348–e01315
Cavalett A, Silva MAC, Toyofuku et al (2017) Dominance of Epsilonproteobacteria associated with a whale fall at a 4204 m depth – South Atlantic Ocean. Deep-Sea Res II 146:53–58. https://doi.org/10.1016/j.dsr2.2017.10.012
Clark MR, Rowden AA, Schlacher T et al (2010) The ecology of seamounts: structure, function, and human impacts. Annu Rev Mar Sci 2:253–278
de Freitas RC, Odisi EJ, Kato C et al (2017) Draft genome sequence of the deep-sea bacterium Moritella sp. JT01 and identification of biotechnologically relevant genes. Mar Biotechnol 19:1–8
DeLong EF, Preston CM, Mincer T et al (2006) Community genomics among stratified microbial assemblages in the ocean’s interior. Science 311:496–503. https://doi.org/10.1126/science.1120250
Di Giulio M (2005) A comparison of proteins from Pyrococcus furiosus and Pyrococcus abyssi: barophily in the physicochemical properties of amino acids and in the genetic code. Gene 346:1–6. https://doi.org/10.1016/j.gene.2004.10.008
Dijkhuizen L, Harder W (1984) Current views on the regulation of autotrophic carbon dioxide fixation via the Calvin cycle in bacteria. Antonie Van Leeuwenhoek 50:473–487. https://doi.org/10.1007/BF02386221
Dinsdale EA, Edwards RA, Hall D et al (2008) Functional metagenomic profiling of nine biomes. Nature 452:629–632. https://doi.org/10.1038/nature06810
Distel DL, Baco AR, Chuang E et al (2000) Do mussels take wooden steps to deep-sea vents? Nature 403:725–726
Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 6:725–740
Ebrahimie E, Ebrahimi M, Sarvestani NR et al (2011) Protein attributes contribute to halo-stability, bioinformatics approach. Saline Syst 7:1–14. https://doi.org/10.1186/1746-1448-7-1
Emerson D, Moyer CL (2010) Microbiology of seamounts: common patterns observed in community structure. Oceanography 23(1):148–163. https://doi.org/10.5670/oceanog.2010.67
Erb TJ (2011) Carboxylases in natural and synthetic microbial pathways. Appl Environ Microbiol 77:8466–8477. https://doi.org/10.1128/AEM.05702-11
Friedrich CG, Rother D, Bardischewsky F (2001) Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl Environ Microbiol 67:2873–2882. https://doi.org/10.1128/aem.67.7.2873-2882.2001
Friedrich CG, Bardischewsky F, Rother D et al (2005) Prokaryotic sulfur oxidation. Curr Opin Microbiol 8:253–259. https://doi.org/10.1016/j.mib.2005.04.005
Friedrich CG, Quentmeier A, Bardischewsky F et al (2007) Microbial sulfur metabolism. Springer-Verlag, Heidelber
Fuhrman JA, Cram JA, Needham DM (2015) Marine microbial community dynamics and their ecological interpretation. Nat Rev Microbiol 13:133–146. https://doi.org/10.1038/nrmicro3417
Fujikura K, Yamanaka T, Sumida PYG et al (2017) Discovery of asphalt seeps in the deep Southwest Atlantic off Brazil. Deep-Sea Res II. https://doi.org/10.1016/j.dsr2.2017.04.002
Gasol J, Pinhassi J, Alonso-Sáez L et al (2008) Towards a better understanding of microbial carbon flux in the sea. Aquat Microb Ecol 53:21–38. https://doi.org/10.3354/ame0130
Gianoulis TA, Raes J, Patel PV et al (2009) Quantifying environmental adaptation of metabolic pathways in metagenomics. Proc Natl Acad Sci U S A 106:1374–1379. https://doi.org/10.1073/pnas.0808022106
Giongo A, Haag T, Simão TLL et al (2016) Discovery of a chemosynthesis-based community in the western South Atlantic Ocean. Deep-Sea Res I 112:45–56. https://doi.org/10.1016/j.dsr.2015.10.010
Goffredi SK, Orphan VJ (2010) Bacterial community shifts in taxa and diversity in response to localized organic loading in the deep sea. Environ Microbiol 12:344–363. https://doi.org/10.1111/j.1462-2920.2009.02072.x
Goffredi SK, Johnson SB, Vrijenhoek RC (2007) Genetic diversity and potential function of microbial symbionts associated with newly discovered species of Osedax polychaete worms. Appl Environ Microbiol 73:2314–2323
Hanson CA, Fuhrman JA, Horner-Devine MC et al (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10:497–506
Herndl GJ, Reinthaler T (2013) Microbial control of the dark end of the biological pump. Nat Geosci 6:718–724. https://doi.org/10.1038/NGEO1921
Herndl GJ, Reinthaler T, Teira E et al (2005) Contribution of Archaea to total prokaryotic production in the Deep Atlantic Ocean. Appl Environ Microbiol 71(5):2303–2309. https://doi.org/10.1128/AEM.71.5
Hügler M, Sievert S (2011) Beyond the Calvin cycle: autotrophic carbon fixation in the ocean. Annu Rev Mar Sci 3:261–289. https://doi.org/10.1146/annurev-marine-120709-142712
Ingalls AE, Shah SR, Hansman RL et al (2006) Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. Proc Natl Acad Sci U S A 103:6442–6447
Jamieson AJ, Fujii T, Mayor DJ et al (2010) Hadal trenches: the ecology of the deepest places on Earth. Trends Ecol Evol 25:190–197
Jiang K, Zhang J, Sakatiku A et al (2018) Discovery and biogeochemistry of asphalt seeps in the North São Paulo Plateau, Brazilian Margin. Sci Rep 8:12619
Jørgensen BB, Boetius A (2007) Feast and famine—microbial life in the deep-sea bed. Nat Rev Microbiol 5:770–781
Jørgensen BB, Marshall IP (2016) Slow microbial life in the seabed. Annu Rev Mar Sci 8:311–332
Jovane L, Hein JR, Yeo IA et al (2019) Multidisciplinary scientific cruise to the Rio Grande Rise. Front Mar Sci 6(252). https://doi.org/10.3389/fmar.2019.00252
Joye SB, Boetius A, Orcutt BN et al (2004) The anaerobic oxidation of methane and sulfate reduction in sediments from Gulf of Mexico cold seeps. Chem Geol 205:219–238
Levin LA (2005) Ecology of cold seep sediments: interactions of fauna with flow, chemistry and microbes. Oceanogr Mar Biol Annu Rev 43:1–46
Longhurst AR (2007) Ecological geography of the sea. Academic, Amsterdam
Lundsten L, Paull CK, Schlining KL et al (2010) Biological characterization of a whale-fall near Vancouver Island, British Columbia, Canada. Deep-Sea Res I 57:918–922. https://doi.org/10.1016/j.dsr.2010.04.006
Manganelli M, Malfatti F, Samo TJ et al (2009) Major role of microbes in carbon fluxes during austral winter in the Southern Drake Passage. PLoS One 4:e6941. https://doi.org/10.1371/journal.pone.0006941
Matz C, Jürgens K (2005) High motility reduces grazing mortality of planktonic bacteria. Appl Environ Microbiol 71:921–929. https://doi.org/10.1128/AEM.71.2.921-929.2005
McNichol J, Stryhanyuk H, Sylva SP et al (2018) Primary productivity below the seafloor at deep-sea hot springs. PNAS 115(26):6756–6761. https://doi.org/10.1073/pnas.1804351115
Medina-Silva R, Oliveira RR, Trindade FJ et al (2017) Microbiota associated with tubes of Escarpia sp. from cold seeps in the southwestern Atlantic Ocean constitutes a community distinct from that of surrounding marine sediment and water. Anton Leeuw Int J G. https://doi.org/10.1007/s10482-017-0975-7
Medina-Silva R, de Oliveira RR, Pivel MAG et al (2018) Microbial diversity from chlorophyll maximum, oxygen minimum and bottom zones in the southwestern Atlantic Ocean. J Mar Syst 178:52–61. https://doi.org/10.1016/j.jmarsys.2017.10.008
Mestre M, Ruiz-González C, Logares R, Duarte CM, Gasol JM, Montserrat Sala M (2018) Sinking particles promote vertical connectivity in the ocean microbiome. PNAS 115(29):E6799–E6807. https://doi.org/10.1073/pnas.1802470115
Middelburg JJ (2011) Chemoautotrophy in the ocean. Geophys Res Lett 38:L24604. https://doi.org/10.1029/2011GL049725
Miller DJ, Ketzer JM, Viana AR et al (2015) Natural gas hydrates in the Rio Grande Cone (Brazil): a new province in the western South Atlantic. Mar Pet Geol 67:187–196. https://doi.org/10.1016/j.marpetgeo.2015.05.012
Molari M, Manini E, Dell’Anno A (2013) Dark inorganic carbon fixation sustains the functioning of benthic deep-sea ecosystems. Glob Biogeochem Cycles 27:212–221. https://doi.org/10.1002/gbc.20030
Montserrat F, Guilhon M, Corrêa PVF et al (2019) Deep-sea mining on the Rio Grande Rise (Southwestern Atlantic): a review on the environmental baseline, ecosystem services and potential impacts. Deep-Sea Res I 145:31–58. https://doi.org/10.1016/j.dsr.2018.12.007
Moses AM, Durbin R (2009) Inferring selection on amino acid preference in protein domains. Mol Biol Evol 26:527–536. https://doi.org/10.1093/molbev/msn286
Nagano Y, Miura T, Nishi S et al (2017) Fungal diversity in deep-sea sediments associated with asphalt seeps at the Sao Paulo Plateau. Deep-Sea Res II. https://doi.org/10.1016/j.dsr2.2017.05.012
Nagata T et al (2010) Emerging concepts on microbial processes in the bathypelagic ocean–ecology, biogeochemistry, and genomics. Deep-Sea Res II 57:1519–1536
Nakagawa S, Takai K, Inagaki F (2005) Distribution, phylogenetic diversity and physiological characteristics of epsilon-Proteobacteria in a deep-sea hydrothermal field. Environ Microbiol 7:1619–1632. https://doi.org/10.1111/j.1462-2920.2005.00856.x
Nunoura T et al (2015) Hadal biosphere: insight into the microbial ecosystem in the deepest ocean on Earth. Proc Natl Acad Sci U S A 112:E1230–E1236
Orcutt BN, Sylvan JB, Knab NJ et al (2011) Microbial ecology of the dark ocean above, at, and below the seafloor. Microbiol Mol Biol Rev 75(2):361–422. https://doi.org/10.1128/MMBR.00039-10
Overmann J, Lepleux C (2016) Marine Bacteria and Archaea: diversity, adaptations, and culturability. In: The marine microbiome. An untapped source of biodiversity and biotechnological potential. Springer, Cham, pp 21–55
Parkes RJ, Cragg B, Roussel E (2014) A review of prokaryotic populations and processes in sub-seafloor sediments, including biosphere: geosphere interactions. Mar Geol 352:409–425. https://doi.org/10.1016/j.margeo.2014.02.009
Peres VF (2016) Diversidade e conectividade de comunidades bacterianas em substratos sintéticos e orgânicos no Atlântico sudoeste profundo. 2016. 95 p. Dissertação (Mestrado em Microbiologia) – Universidade de São Paulo, São Paulo
Pop Ristova P, Wenzhofer F, Ramette A (2014) Spatial scales of bacterial community diversity at cold seeps (Eastern Mediterranean Sea). ISME J 9:1306–1318. https://doi.org/10.1038/ismej.2014.217
Queiroz LL, Bendia AG, Duarte RTD et al (2020) Bacterial diversity in deep-sea sediments under influence of asphalt seep at the São Paulo Plateau. Anton Leeuw Int J G. https://doi.org/10.1007/s10482-020-01384-8
Raes J, Letunic I, Yamada T et al (2011) Toward molecular trait-based ecology through integration of biogeochemical, geographical and metagenomic data. Mol Syst Biol 7:473. https://doi.org/10.1038/msb.2011.6
Reed CJ, Lewis H, Trejo E (2013) Protein adaptations in archaeal extremophiles. Archaea. https://doi.org/10.1155/2013/373275
Reinthaler T, van Aken HM, Herndl GJ (2010) Major contribution of autotrophy to microbial carbon cycling in the deep North Atlantic’s interior. Deep Sea Res II Top Stud Oceanogr 57:1572. https://doi.org/10.1016/j.dsr2.2010.02.023
Salazar G, Cornejo-Castillo FM, Benítez-Barrios V et al (2016) Global diversity and biogeography of deep-sea pelagic prokaryotes. ISME J 10:596–608. https://doi.org/10.1038/ismej.2015.137
Santoro AE, Richter RA, Dupont CL (2019) Planktonic Marine Archaea. Annu Rev Mar Sci 11:131–158
Schulz HD, Zabel M (2006) Marine geochemistry, 2nd edn. Springer-Verlag, Berlin, 414 p
Sheik CS, Jain S, Dick GJ (2014) Metabolic flexibility of enigmatic SAR324 revealed through metagenomics and metatranscriptomics. Environ Microbiol 16:304–317. https://doi.org/10.1111/1462-2920.12165
Shimabukuro M, Alfaro-Lucas JM, Bernardino AF et al (this volume) Chapter 5: Chemosynthetic ecosystems on the Brazilian Deep-Sea margin. In: Sumida PYG, Bernardino AF, DeLeo FC (eds) Brazilian Deep-Sea biodiversity. Springer Nature, Cham
Signori CN (2014) Chemosynthesis and bacterial production in marine ecosystems: quantification, importance and regulatory factors. PhD thesis, Federal University of Rio de Janeiro, Brazil. 176 p
Sintes E, De Corte D, Haberleitner E, Herndl GJ (2016) Geographic distribution of archaeal ammonia oxidizing ecotypes in the Atlantic Ocean. Front Microbiol 7:77. https://doi.org/10.3389/fmicb.2016.00077
Sjöstedt J, Martiny JB, Munk P et al (2014) Abundance of broad bacterial taxa in the Sargasso Sea explained by environmental conditions but not water mass. Appl Environ Microbiol 80:2786–2795
Smith CR (2012) Chemosynthesis in the deep-sea: life without the sun. Biogeosci Discuss 9:17037–17052. https://doi.org/10.5194/bgd-9-17037-2012
Smith CR, Baco AR (2003) Ecology of whale falls at the deep-sea floor. Oceanogr Mar Biol 41:311–354
Smith CR, Kukert H, Wheatcroft RA et al (1989) Vent fauna on whale remains. Nature 341:27–28. https://doi.org/10.1038/341027a0
Smith CR, De Leo FC, Bernardino AF et al (2008) Abyssal food limitation, ecosystem structure and climate change. Trends Ecol Evol 23:518–528
Smith CR, Bernardino AF, Baco A (2014) Seven-year enrichment: macrofaunal succession in deep-sea sediments around a 30 tonne whale fall in the Northeast Pacific. Mar Ecol Prog Ser 515:133–149. doi.org/10.3354/meps10955
Smith CR, Glover AG, Treude T, Higgs ND, Amon DJ (2015) Whale-fall ecosystems: recent insights into ecology, paleoecology, and evolution. Annu Rev Mar Sci 7:571–596. https://doi.org/10.1146/annurev-marine-010213-135144
Stocker R (2012) Marine microbes see a sea of gradients. Science 338:628–633
Sumida PYG, Alfaro-Lucas JM, Shimabukuro M et al (2016) Deep-sea whale fall fauna from the Atlantic resembles that of the Pacific Ocean. Sci Rep 6:22139. https://doi.org/10.1038/srep22139
Sunagawa S, Coelho LP, Chaffron S et al (2015) Structure and function of the global ocean microbiome. Science 348:1261359–1261359. https://doi.org/10.1126/science.1261359
Swan SB, Martinez-Garcia M, Preston CM et al (2011) Potential for chemolithoautotrophy among ubiquitous bacteria lineages in the dark ocean. Science 333:1296–1300. https://doi.org/10.1126/science.1203690
Taylor GT, Iabichella M, Ho T-Y et al (2001) Chemoautotrophy in the redox transition zone of the Cariaco Basin: a significant midwater source of organic carbon production. Limnol Oceanogr 46:148–163. https://doi.org/10.4319/lo.2001.46.1.0148
Treude T, Smith CR, Wenzhöfer F (2009) Biogeochemistry of a deep-sea whale fall: sulfate reduction, sulfide efflux and methanogenesis. Mar Ecol Prog Ser 382:1–21. https://doi.org/10.3354/meps07972
Tringe SG, Mering CV, Kobayashi et al (2005) Comparative metagenomics of microbial communities. Science 308:554–557. https://doi.org/10.1126/science.1107851
Turner JT (2015) Zooplankton fecal pellets, marine snow, phytodetritus and the ocean’s biological pump. Prog Oceanogr 130:205–248. https://doi.org/10.1016/j.pocean.2014.08.005
Tyler PA (2003) Ecosystems of the deep Oceans, vol 28. Elsevier, Amsterdam/Boston
Ulloa O, Canfield DE, DeLong EF et al (2012) Microbial oceanography of anoxic oxygen minimum zones. Proc Natl Acad Sci U S A. https://doi.org/10.1073/pnas.1205009109
Walsh DA et al (2009) Metagenome of a versatile chemolithoautotroph from expanding oceanic dead zones. Science 326:578–582. https://doi.org/10.1126/science.1175309
Watling L, Guinotte J, Clark MR et al (2013) A proposed biogeography of the deep ocean floor. Prog Oceanogr 111:91–112
Wright JJ, Konwar KM, Hallam SJ (2012) Microbial ecology of expanding oxygen minimum zones. Nat Rev Microbiol 10:381–394. https://doi.org/10.1038/nrmicro2778
Yamamoto M, Nakagawa S, Shimamura S et al (2010) Molecular characterization of inorganic sulfur-compound metabolism in the deep-sea epsilonproteobacterium Sulfurovum sp. NBC37-1. Environ Microbiol 12:1144–1153. https://doi.org/10.1111/j.1462-2920.2010.02155.x
Acknowledgments
The authors are thankful to the Brazilian agencies: São Paulo Research Foundation (Biota/FAPESP 2011/50185-1 and FAPESP 2014/50820-7), Foundation for Research and Innovation of the State of Santa Catarina (FAPESC 3422/2012), Coordination for the Improvement of Higher Education Personnel (CAPES/JSPS 02/13), and National Council for Scientific and Technological Development (CNPq - INCT-Mar COI, Process 565062/2010-7), as well as to Iatá-Piúna initiative for supporting this work. We also thank CAPES (Process 08740/14-3) and CNPq (Process 311010/2015-6) for scholarships provided to AOSL. CNS received a Post Doc fellowship (FAPESP 2016/16183-5).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2020 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Signori, C.N., Lima, A.O.d., Nakayama, C.R., Pellizari, V.H. (2020). Deep-Sea Microbes in the Southwestern Atlantic. In: Sumida, P.Y.G., Bernardino, A.F., De Léo, F.C. (eds) Brazilian Deep-Sea Biodiversity. Brazilian Marine Biodiversity . Springer, Cham. https://doi.org/10.1007/978-3-030-53222-2_6
Download citation
DOI: https://doi.org/10.1007/978-3-030-53222-2_6
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-53221-5
Online ISBN: 978-3-030-53222-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)