Biogeography of Southern Ocean Prokaryotes: a Comparison of the Indian and Pacific Sectors

Overview

Journal Environ Microbiol

Specialties Environmental Health
Microbiology

Date 2022 Jan 20

PMID 35049099

Authors

Swan L S Sow

Mark V Brown

Laurence J Clarke

Andrew Bissett

Jodie van de Kamp

Thomas W Trull

Eric J Raes

Justin R Seymour

Anna R Bramucci

Martin Ostrowski

Philip W Boyd

Bruce E Deagle

Paula C Pardo

Bernadette M Sloyan

Levente Bodrossy

Affiliations

Soon will be listed here.

Abstract

We investigated the Southern Ocean (SO) prokaryote community structure via zero-radius operational taxonomic unit (zOTU) libraries generated from 16S rRNA gene sequencing of 223 full water column profiles. Samples reveal the prokaryote diversity trend between discrete water masses across multiple depths and latitudes in Indian (71-99°E, summer) and Pacific (170-174°W, autumn-winter) sectors of the SO. At higher taxonomic levels (phylum-family) we observed water masses to harbour distinct communities across both sectors, but observed sectorial variations at lower taxonomic levels (genus-zOTU) and relative abundance shifts for key taxa such as Flavobacteria, SAR324/Marinimicrobia, Nitrosopumilus and Nitrosopelagicus at both epi- and bathy-abyssopelagic water masses. Common surface bacteria were abundant in several deep-water masses and vice-versa suggesting connectivity between surface and deep-water microbial assemblages. Bacteria from same-sector Antarctic Bottom Water samples showed patchy, high beta-diversity which did not correlate well with measured environmental parameters or geographical distance. Unconventional depth distribution patterns were observed for key archaeal groups: Crenarchaeota was found across all depths in the water column and persistent high relative abundances of common epipelagic archaeon Nitrosopelagicus was observed in deep-water masses. Our findings reveal substantial regional variability of SO prokaryote assemblages that we argue should be considered in wide-scale SO ecosystem microbial modelling.

Citing Articles

Seasonal dynamics and diversity of Antarctic marine viruses reveal a novel viral seascape.

Piedade G, Schon M, Lood C, Fofanov M, Wesdorp E, Biggs T Nat Commun. 2024; 15(1):9192.

PMID: 39448562 PMC: 11502894. DOI: 10.1038/s41467-024-53317-y.

Unveiling the microbial diversity across the northern Ninety East Ridge in the Indian Ocean.

Li D, Wang L, Jiang F, Zeng X, Xu Q, Zhang X Front Microbiol. 2024; 15:1436735.

PMID: 39380675 PMC: 11458393. DOI: 10.3389/fmicb.2024.1436735.

Habitat specificity modulates the bacterial biogeographic patterns in the Southern Ocean.

Delleuze M, Schwob G, Orlando J, Gerard K, Saucede T, Brickle P FEMS Microbiol Ecol. 2024; 100(11).

PMID: 39363207 PMC: 11523047. DOI: 10.1093/femsec/fiae134.

Picoplankton diversity in an oligotrophic and high salinity environment in the central Adriatic Sea.

Santic D, Stojan I, Matic F, Trumbic Z, Vrdoljak Tomas A, Fredotovic Z Sci Rep. 2023; 13(1):7617.

PMID: 37165047 PMC: 10172355. DOI: 10.1038/s41598-023-34704-9.

References

Beaugrand G, Kirby R . How Do Marine Pelagic Species Respond to Climate Change? Theories and Observations. Ann Rev Mar Sci. 2018; 10:169-197. DOI: 10.1146/annurev-marine-121916-063304. View

Lopez-Garcia P, Lopez-Lopez A, Moreira D, Rodriguez-Valera F . Diversity of free-living prokaryotes from a deep-sea site at the Antarctic Polar Front. FEMS Microbiol Ecol. 2001; 36(2-3):193-202. DOI: 10.1016/s0168-6496(01)00133-7. View

Mestre M, Ruiz-Gonzalez C, Logares R, Duarte C, Gasol J, Sala M . Sinking particles promote vertical connectivity in the ocean microbiome. Proc Natl Acad Sci U S A. 2018; 115(29):E6799-E6807. PMC: 6055141. DOI: 10.1073/pnas.1802470115. View

Galand P, Potvin M, Casamayor E, Lovejoy C . Hydrography shapes bacterial biogeography of the deep Arctic Ocean. ISME J. 2009; 4(4):564-76. DOI: 10.1038/ismej.2009.134. View

Grzymski J, Riesenfeld C, Williams T, Dussaq A, Ducklow H, Erickson M . A metagenomic assessment of winter and summer bacterioplankton from Antarctica Peninsula coastal surface waters. ISME J. 2012; 6(10):1901-15. PMC: 3446801. DOI: 10.1038/ismej.2012.31. View

Gilbert J, Steele J, Caporaso J, Steinbruck L, Reeder J, Temperton B . Defining seasonal marine microbial community dynamics. ISME J. 2011; 6(2):298-308. PMC: 3260500. DOI: 10.1038/ismej.2011.107. View

Raes E, Bodrossy L, van de Kamp J, Bissett A, Ostrowski M, Brown M . Oceanographic boundaries constrain microbial diversity gradients in the South Pacific Ocean. Proc Natl Acad Sci U S A. 2018; 115(35):E8266-E8275. PMC: 6126737. DOI: 10.1073/pnas.1719335115. View

Giovannoni S, Vergin K . Seasonality in ocean microbial communities. Science. 2012; 335(6069):671-6. DOI: 10.1126/science.1198078. View

Wilkins D, Lauro F, Williams T, DeMaere M, Brown M, Hoffman J . Biogeographic partitioning of Southern Ocean microorganisms revealed by metagenomics. Environ Microbiol. 2012; 15(5):1318-33. DOI: 10.1111/1462-2920.12035. View

10.

Brown M, van de Kamp J, Ostrowski M, Seymour J, Ingleton T, Messer L . Systematic, continental scale temporal monitoring of marine pelagic microbiota by the Australian Marine Microbial Biodiversity Initiative. Sci Data. 2018; 5:180130. PMC: 6049030. DOI: 10.1038/sdata.2018.130. View

11.

Alcaman-Arias M, Farias L, Verdugo J, Alarcon-Schumacher T, Diez B . Microbial activity during a coastal phytoplankton bloom on the Western Antarctic Peninsula in late summer. FEMS Microbiol Lett. 2018; 365(10). DOI: 10.1093/femsle/fny090. View

12.

Wilkins D, van Sebille E, Rintoul S, Lauro F, Cavicchioli R . Advection shapes Southern Ocean microbial assemblages independent of distance and environment effects. Nat Commun. 2013; 4:2457. DOI: 10.1038/ncomms3457. View

13.

Field K, Gordon D, Wright T, Rappe M, Urback E, Vergin K . Diversity and depth-specific distribution of SAR11 cluster rRNA genes from marine planktonic bacteria. Appl Environ Microbiol. 1997; 63(1):63-70. PMC: 168303. DOI: 10.1128/aem.63.1.63-70.1997. View

14.

Giebel H, Kalhoefer D, Lemke A, Thole S, Gahl-Janssen R, Simon M . Distribution of Roseobacter RCA and SAR11 lineages in the North Sea and characteristics of an abundant RCA isolate. ISME J. 2010; 5(1):8-19. PMC: 3105675. DOI: 10.1038/ismej.2010.87. View

15.

Smith Jr K, Ruhl H, Huffard C, Messie M, Kahru M . Episodic organic carbon fluxes from surface ocean to abyssal depths during long-term monitoring in NE Pacific. Proc Natl Acad Sci U S A. 2018; 115(48):12235-12240. PMC: 6275536. DOI: 10.1073/pnas.1814559115. View

16.

Manganelli M, Malfatti F, Samo T, Mitchell B, Wang H, Azam F . Major role of microbes in carbon fluxes during Austral winter in the Southern Drake Passage. PLoS One. 2009; 4(9):e6941. PMC: 2736376. DOI: 10.1371/journal.pone.0006941. View

17.

Sintes E, Bergauer K, De Corte D, Yokokawa T, Herndl G . Archaeal amoA gene diversity points to distinct biogeography of ammonia-oxidizing Crenarchaeota in the ocean. Environ Microbiol. 2012; 15(5):1647-58. PMC: 3712475. DOI: 10.1111/j.1462-2920.2012.02801.x. View

18.

Giovannoni S . SAR11 Bacteria: The Most Abundant Plankton in the Oceans. Ann Rev Mar Sci. 2016; 9:231-255. DOI: 10.1146/annurev-marine-010814-015934. View

19.

Cram J, Chow C, Sachdeva R, Needham D, Parada A, Steele J . Seasonal and interannual variability of the marine bacterioplankton community throughout the water column over ten years. ISME J. 2014; 9(3):563-80. PMC: 4331575. DOI: 10.1038/ismej.2014.153. View

20.

Varela M, van Aken H, Sintes E, Herndl G . Latitudinal trends of Crenarchaeota and Bacteria in the meso- and bathypelagic water masses of the Eastern North Atlantic. Environ Microbiol. 2008; 10(1):110-24. DOI: 10.1111/j.1462-2920.2007.01437.x. View