Vertical microbial profiling of water column reveals prokaryotic communities and distribution features of Antarctic Peninsula

Jiang Li; Luying Zhao; Xiaoqian Gu; Chengxuan Li; Qian Zhang; Liping Fu; Ao Zhang

doi:10.1007/s13131-023-2160-3

Volume 42 Issue 9

Sep. 2023

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Jiang Li, Luying Zhao, Xiaoqian Gu, Chengxuan Li, Qian Zhang, Liping Fu, Ao Zhang. Vertical microbial profiling of water column reveals prokaryotic communities and distribution features of Antarctic Peninsula[J]. Acta Oceanologica Sinica, 2023, 42(9): 90-100. doi: 10.1007/s13131-023-2160-3

Citation:

Jiang Li, Luying Zhao, Xiaoqian Gu, Chengxuan Li, Qian Zhang, Liping Fu, Ao Zhang. Vertical microbial profiling of water column reveals prokaryotic communities and distribution features of Antarctic Peninsula[J]. Acta Oceanologica Sinica, 2023, 42(9): 90-100. doi: 10.1007/s13131-023-2160-3

Citation:

Jiang Li, Luying Zhao, Xiaoqian Gu, Chengxuan Li, Qian Zhang, Liping Fu, Ao Zhang. Vertical microbial profiling of water column reveals prokaryotic communities and distribution features of Antarctic Peninsula[J]. Acta Oceanologica Sinica, 2023, 42(9): 90-100. doi: 10.1007/s13131-023-2160-3

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Vertical microbial profiling of water column reveals prokaryotic communities and distribution features of Antarctic Peninsula

doi: 10.1007/s13131-023-2160-3

Jiang Li^{1, 2
,
,},
Luying Zhao^{1, 2},
Xiaoqian Gu³,
Chengxuan Li^{1, 2},
Qian Zhang^{1, 2},
Liping Fu^{1, 2},
Ao Zhang⁴

1.
Marine Biological Resources and Environment Center, First Institute of Oceanography, Ministry of Natural Resources, Qingdao 266061, China
2.
Ministry of Natural Resources Key Labatary for Science & Technology of Marine Ecosystems, Qingdao 266061, China
3.
CAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
4.
College of Chemical Engineering, Qingdao University of Science & Technology, Qingdao 266042, China

Funds: The Impact and Response of Antarctic Seas to Climate Change under contract No. IRFSOCC2020-2022.

More Information

Corresponding author: E-mail: lijiang@fio.org.cn
Received Date: 2022-06-20
Accepted Date: 2022-11-17

Available Online: 2023-10-16

Publish Date: 2023-09-01

Abstract

Abstract

Prokaryotic diversity and community composition in the water column of eight stations (63 samples) around the Antarctic Peninsula of the Southern Ocean were investigated. Through pyrosequencing of the V3–V4 hypervariable regions of the 16S ribosomal RNA gene, we characterized 4 720 089 valid reads representing 48 188 operational taxonomic units (OTUs, 97% similarity). The community was dominated by the phyla Pseudomonadota (original name: Proteobacteria, 47%), Oxyphotobacteria (26%), and Bacteroidota (original name: Bacteroidetes, 18%), which comprised an average of 91% of the total OTUs in all samples. The prokaryotic community composition varied vertically within the water column. Water column prokaryotic communities exhibited a clear depth profile, with higher microbial richness and higher diversity observed with increasing water depth. Cluster analysis of the community composition of water column samples exhibited a similar trend with depth. Correlation with environmental factors suggested distinct variation in prokaryotic community composition with changes in depth, salinity, temperature and dissolved oxygen levels. Functional prediction showed presence of active nitrogen, sulphur and methane metabolic cycles along the vertical transect of the studied region. These results will improve our knowledge of prokaryotic diversity and community composition at different depth of water column for better understanding of the microbial ecology and nutrient cycles in Antarctic Peninsula region of the Southern Ocean.
- prokaryotic diversity,
- 16S rRNA,
- high-throughput sequencing (HTS),
- Southern Ocean

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References(71)

References

Abell G C J, Bowman J P. 2005. Ecological and biogeographic relationships of class Flavobacteria in the Southern Ocean. FEMS Microbiology Ecology, 51(2): 265–277. doi: 10.1016/j.femsec.2004.09.001

Agogué H, Lamy D, Neal P R, et al. 2011. Water mass-specificity of bacterial communities in the North Atlantic revealed by massively parallel sequencing. Molecular Ecology, 20(2): 258–274. doi: 10.1111/j.1365-294X.2010.04932.x

Aislabie J M, Jordan S, Barker G M. 2008. Relation between soil classification and bacterial diversity in soils of the Ross Sea region, Antarctica. Geoderma, 144(1−2): 9–20. doi: 10.1016/j.geoderma.2007.10.006

Aldunate M, De la Iglesia R, Bertagnolli A D, et al. 2018. Oxygen modulates bacterial community composition in the coastal upwelling waters off central Chile. Deep-Sea Research Part II: Topical Studies in Oceanography, 156: 68–79. doi: 10.1016/j.dsr2.2018.02.001

Beman J M, Carolan M T. 2013. Deoxygenation alters bacterial diversity and community composition in the ocean’s largest oxygen minimum zone. Nature Communications, 4: 2705. doi: 10.1038/ncomms3705

Brown M V, Lauro F M, DeMaere M Z, et al. 2012. Global biogeography of SAR11 marine bacteria. Molecular Systems Biology, 8: 595. doi: 10.1038/msb.2012.28

Brown M V, Philip G K, Bunge J A, et al. 2009. Microbial community structure in the North Pacific Ocean. The ISME Journal, 3(12): 1374–1386. doi: 10.1038/ismej.2009.86

Bryant J A, Stewart F J, Eppley J M, et al. 2012. Microbial community phylogenetic and trait diversity declines with depth in a marine oxygen minimum zone. Ecology, 93(7): 1659–1673. doi: 10.1890/11-1204.1

Caporaso J G, Kuczynski J, Stombaugh J, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5): 335–336. doi: 10.1038/nmeth.f.303

Chong C W, Dunn M J, Convey P, et al. 2009a. Environmental influences on bacterial diversity of soils on Signy Island, maritime Antarctic. Polar Biology, 32(11): 1571–1582. doi: 10.1007/s00300-009-0656-8

Chong C W, Goh Y S, Convey P, et al. 2013. Spatial pattern in Antarctica: what can we learn from Antarctic bacterial isolates?. Extremophiles, 17(5): 733–745

Chong C W, Tan G Y A, Wong R C S, et al. 2009b. DGGE fingerprinting of bacteria in soils from eight ecologically different sites around Casey Station, Antarctica. Polar Biology, 32(6): 853–860. doi: 10.1007/s00300-009-0585-6

Cleary D F R, de Voogd N J, Polónia A R M, et al. 2015. Composition and predictive functional analysis of bacterial communities in seawater, sediment and sponges in the Spermonde Archipelago, Indonesia. Microbial Ecology, 70(4): 889–903. doi: 10.1007/s00248-015-0632-5

DeLong E F, Preston C M, Mincer T, et al. 2006. Community genomics among stratified microbial assemblages in the ocean’s interior. Science, 311(5760): 496–503. doi: 10.1126/science.1120250

Dinasquet J, Richert I, Logares R, et al. 2017. Mixing of water masses caused by a drifting iceberg affects bacterial activity, community composition and substrate utilization capability in the Southern Ocean. Environmental Microbiology, 19(6): 2453–2467. doi: 10.1111/1462-2920.13769

Ducklow H W, Myers K M S, Erickson M, et al. 2011. Response of a summertime Antarctic marine bacterial community to glucose and ammonium enrichment. Aquatic Microbial Ecology, 64(3): 205–220. doi: 10.3354/ame01519

Esper O, Zonneveld K A F. 2002. Distribution of organic-walled dinoflagellate cysts in surface sediments of the Southern Ocean (eastern Atlantic sector) between the Subtropical Front and the Weddell Gyre. Marine Micropaleontology, 46(1−2): 177–208. doi: 10.1016/S0377-8398(02)00041-5

Fandino L B, Riemann L, Steward G F, et al. 2001. Variations in bacterial community structure during a dinoflagellate bloom analyzed by DGGE and 16S rDNA sequencing. Aquatic Microbial Ecology, 23(2): 119–130

Fierer N, Breitbart M, Nulton J, et al. 2007. Metagenomic and small-subunit rRNA analyses reveal the genetic diversity of bacteria, archaea, fungi, and viruses in soil. Applied and Environmental Microbiology, 73(21): 7059–7066. doi: 10.1128/AEM.00358-07

Francis C A, Beman J M, Kuypers M M M. 2007. New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. The ISME Journal, 1(1): 19–27. doi: 10.1038/ismej.2007.8

Fuhrman J A, Cram J A, Needham D M. 2015. Marine microbial community dynamics and their ecological interpretation. Nature Reviews Microbiology, 13(3): 133–146. doi: 10.1038/nrmicro3417

Ghiglione J F, Galand P E, Pommier T, et al. 2012. Pole-to-pole biogeography of surface and deep marine bacterial communities. Proceedings of the National Academy of Sciences, 109(43): 17633–17638. doi: 10.1073/pnas.1208160109

Ghiglione J F, Murray A E. 2012. Pronounced summer to winter differences and higher wintertime richness in coastal Antarctic marine bacterioplankton. Environmental Microbiology, 14(3): 617–629. doi: 10.1111/j.1462-2920.2011.02601.x

Giovannoni S J, Stingl U. 2005. Molecular diversity and ecology of microbial plankton. Nature, 437(7057): 343–348. doi: 10.1038/nature04158

Giovannoni S J, Vergin K L. 2012. Seasonality in ocean microbial communities. Science, 335(6069): 671–676. doi: 10.1126/science.1198078

Goffredi S K, Waren A, Orphan V J, et al. 2004. Novel forms of structural integration between microbes and a hydrothermal vent gastropod from the Indian Ocean. Applied and Environmental Microbiology, 70(5): 3082–3090. doi: 10.1128/AEM.70.5.3082-3090.2004

Grzymski J J, Riesenfeld C S, Williams T J, et al. 2012. A metagenomic assessment of winter and summer bacterioplankton from Antarctica Peninsula coastal surface waters. The ISME Journal, 6(10): 1901–1915. doi: 10.1038/ismej.2012.31

Hammer Ø, Harper D A T, Ryan P D. 2001. PAST: Palaeontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica, 4(1): 1–9

Hartmann M, Gomez-Pereira P, Grob C, et al. 2014. Efficient CO₂ fixation by surface Prochlorococcus in the Atlantic Ocean. The ISME Journal, 8(11): 2280–2289

Jamieson R E, Rogers A D, Billett D S M, et al. 2012. Patterns of marine bacterioplankton biodiversity in the surface waters of the Scotia Arc, Southern Ocean. FEMS Microbiology Ecology, 80(2): 452–468. doi: 10.1111/j.1574-6941.2012.01313.x

Jayakumar A, Chang B X, Widner B, et al. 2017. Biological nitrogen fixation in the oxygen-minimum region of the eastern tropical North Pacific Ocean. The ISME Journal, 11(10): 2356–2367. doi: 10.1038/ismej.2017.97

Karlson A M L, Duberg J, Motwani N H, et al. 2015. Nitrogen fixation by cyanobacteria stimulates production in Baltic food webs. AMBIO, 44(S3): 413–426. doi: 10.1007/s13280-015-0660-x

Kembel S W, Eisen J A, Pollard K S, et al. 2011. The phylogenetic diversity of metagenomes. PLoS ONE, 6(8): e23214. doi: 10.1371/journal.pone.0023214

Landa M, Blain S, Christaki U, et al. 2016. Shifts in bacterial community composition associated with increased carbon cycling in a mosaic of phytoplankton blooms. The ISME Journal, 10(1): 39–50. doi: 10.1038/ismej.2015.105

Laws E A, Falkowski P G, Smith Jr W O, et al. 2000. Temperature effects on export production in the open ocean. Global Biogeochemical Cycles, 14(4): 1231–1246. doi: 10.1029/1999GB001229

Liu Ning, Zhou Jialiang, Han Lujia, et al. 2017. Role and multi-scale characterization of bamboo biochar during poultry manure aerobic composting. Bioresource Technology, 241: 190–199. doi: 10.1016/j.biortech.2017.03.144

Loescher C R, Großkopf T, Desai F D, et al. 2014. Facets of diazotrophy in the oxygen minimum zone waters off Peru. The ISME Journal, 8(11): 2180–2192. doi: 10.1038/ismej.2014.71

Manganelli M, Malfatti F, Samo T J, et al. 2009. Major role of microbes in carbon fluxes during austral winter in the southern drake passage. PLoS ONE, 4(9): e6941. doi: 10.1371/journal.pone.0006941

Mincer T J, Church M J, Taylor L T, et al. 2007. Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific subtropical gyre. Environmental Microbiology, 9(5): 1162–1175. doi: 10.1111/j.1462-2920.2007.01239.x

Murray A E, Grzymski J J. 2007. Diversity and genomics of Antarctic marine micro-organisms. Philosophical Transactions of the Royal Society B: Biological Sciences, 362(1488): 2259–2271. doi: 10.1098/rstb.2006.1944

Murray A E, Peng V, Tyler C, et al. 2011. Marine bacterioplankton biomass, activity and community structure in the vicinity of Antarctic icebergs. Deep-Sea Research Part II: Topical Studies in Oceanography, 58(11−12): 1407–1421. doi: 10.1016/j.dsr2.2010.11.021

Nakagawa S, Takai K, Inagaki F, et al. 2005. Distribution, phylogenetic diversity and physiological characteristics of epsilon-Proteobacteria in a deep-sea hydrothermal field. Environmental Microbiology, 7(10): 1619–1632. doi: 10.1111/j.1462-2920.2005.00856.x

Oren A, Garrity G M. 2021. Valid publication of the names of forty-two phyla of prokaryotes. International Journal of Systematic and Evolutionary Microbiology, 71(10): 005056

Park P K. 1969. A practical handbook of seawater analysis. Fisheries Research Board of Canada Bulletin 167. J. D. H. Strickland, T. R. Parsons. The Quarterly Review of Biology , 44 (3): 327.

Pommier T, Neal P R, Gasol J M, et al. 2010. Spatial patterns of bacterial richness and evenness in the NW Mediterranean Sea explored by pyrosequencing of the 16S rRNA. Aquatic Microbial Ecology, 61(3): 221–233. doi: 10.3354/ame01484

R D Core Team. 2008. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org, ISBN 3-900051-07-0"[2022-03-21/2022-03-23]

Segata N, Izard J, Waldron L, et al. 2011. Metagenomic biomarker discovery and explanation. Genome Biology, 12(6): R60. doi: 10.1186/gb-2011-12-6-r60

Selje N, Simon M, Brinkhoff T. 2004. A newly discovered Roseobacter cluster in temperate and polar oceans. Nature, 427(6973): 445–448. doi: 10.1038/nature02272

Shivaji S, Kumari K, Kishore K H, et al. 2011. Vertical distribution of bacteria in a lake sediment from Antarctica by culture-independent and culture-dependent approaches. Research in Microbiology, 162(2): 191–203. doi: 10.1016/j.resmic.2010.09.020

Swan B K, Martinez-Garcia M, Preston C M, et al. 2011. Potential for chemolithoautotrophy among ubiquitous bacteria lineages in the dark ocean. Science, 333(6047): 1296–1300. doi: 10.1126/science.1203690

The Human Microbiome Project Consortium. 2012. Structure, function and diversity of the healthy human microbiome. Nature, 486(7402): 207–214. doi: 10.1038/nature11234

Thomas F, Hehemann J H, Rebuffet E, et al. 2011. Environmental and gut Bacteroidetes: the food connection. Frontiers in Microbiology, 2: 93

Torstensson A, Dinasquet J, Chierici M, et al. 2015. Physicochemical control of bacterial and protist community composition and diversity in Antarctic sea ice. Environmental Microbiology, 17(10): 3869–3881. doi: 10.1111/1462-2920.12865

Treusch A H, Vergin K L, Finlay L A, et al. 2009. Seasonality and vertical structure of microbial communities in an ocean gyre. The ISME Journal, 3(10): 1148–1163. doi: 10.1038/ismej.2009.60

Venkatachalam S, Matcher G F, Lamont T, et al. 2019. Influence of oceanographic variability on near-shore microbial communities of the sub-Antarctic Prince Edward Islands. Limnology and Oceanography, 64(1): 258–271. doi: 10.1002/lno.11035

Venter J C, Remington K, Heidelberg J F, et al. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science, 304(5667): 66–74. doi: 10.1126/science.1093857

Walsh E A, Kirkpatrick J B, Rutherford S D, et al. 2016. Bacterial diversity and community composition from seasurface to subseafloor. The ISME Journal, 10(4): 979–989. doi: 10.1038/ismej.2015.175

Walsh E A, Smith D C, Sogin M L, et al. 2015. Bacterial and archaeal biogeography of the deep chlorophyll maximum in the South Pacific Gyre. Aquatic Microbial Ecology, 75(1): 1–13. doi: 10.3354/ame01746

Ward B B. 1996. Nitrification and ammonification in aquatic systems. Life Support and Biosphere Science: International Journal of Earth Space, 3: 25–29

Ward P, Whitehouse M, Brandon M, et al. 2003. Mesozooplankton community structure across the Antarctic Circumpolar Current to the north of South Georgia: Southern Ocean. Marine Biology, 143(1): 121–130. doi: 10.1007/s00227-003-1019-6

West N J, Obernosterer I, Zemb O, et al. 2008. Major differences of bacterial diversity and activity inside and outside of a natural iron-fertilized phytoplankton bloom in the Southern Ocean. Environmental Microbiology, 10(3): 738–756. doi: 10.1111/j.1462-2920.2007.01497.x

Wilkins D, Lauro F M, Williams T J, et al. 2013a. Biogeographic partitioning of Southern Ocean microorganisms revealed by metagenomics. Environmental Microbiology, 15(5): 1318–1333. doi: 10.1111/1574-6976.12007

Wilkins D, van Sebille E, Rintoul S R, et al. 2013b. Advection shapes Southern Ocean microbial assemblages independent of distance and environment effects. Nature Communications, 4: 2457. doi: 10.1038/ncomms3457

Wilkins D, Yau S, Williams T J, et al. 2012. Key microbial drivers in Antarctic aquatic environments. FEMS Microbiology Reviews, 37(3): 303–335

Williams T J, Long E, Evans F, et al. 2012. A metaproteomic assessment of winter and summer bacterioplankton from Antarctic Peninsula coastal surface waters. The ISME Journal, 6(10): 1883–1900. doi: 10.1038/ismej.2012.28

Wright J J, Konwar K M, Hallam S J. 2012. Microbial ecology of expanding oxygen minimum zones. Nature Reviews Microbiology, 10(6): 381–394. doi: 10.1038/nrmicro2778

Yergeau E, Bokhorst S, Huiskes A H L, et al. 2007a. Size and structure of bacterial, fungal and nematode communities along an Antarctic environmental gradient. FEMS Microbiology Ecology, 59(2): 436–451

Yergeau E, Bokhorst S, Kang Sanghoon, et al. 2012. Shifts in soil microorganisms in response to warming are consistent across a range of Antarctic environments. The ISME Journal, 6(3): 692–702. doi: 10.1038/ismej.2011.124

Yergeau E, Kang Sanghoon, He Zhili, et al. 2007b. Functional microarray analysis of nitrogen and carbon cycling genes across an Antarctic latitudinal transect. The ISME Journal, 1(2): 163–179. doi: 10.1038/ismej.2007.24

Yergeau E, Newsham K K, Pearce D A, et al. 2007c. Patterns of bacterial diversity across a range of Antarctic terrestrial habitats. Environmental Microbiology, 9(11): 2670–2682. doi: 10.1111/j.1462-2920.2007.01379.x

Zinger L, Amaral-Zettler L A, Fuhrman J A, et al. 2011. Global patterns of bacterial beta-diversity in seafloor and seawater ecosystems. PLoS ONE, 6(9): e24570. doi: 10.1371/journal.pone.0024570

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