Marine microbial communities vary seasonally and spatially, but these two factors are rarely addressed together. In this study, the temporal and spatial patterns of the bacterial and archaeal community were studied along a coast-to-offshore transect in the Eastern Mediterranean Sea (EMS) over six cruises, in three seasons of 2 consecutive years. Amplicon sequencing of 16S rRNA genes and transcripts was performed to determine presence and activity, respectively. The ultra-oligotrophic status of the Southeastern Mediterranean Sea was reflected in the microbial community composition dominated by oligotrophic bacterial groups such as SAR11, even at the most coastal station sampled, throughout the year. Seasons significantly affected the microbial communities, explaining more than half of the observed variability. However, the same few taxa dominated the community over the 2-year sampling period, varying only in their degree of dominance. While there was no overall effect of station location on the microbial community, the most coastal site (16 km offshore) differed significantly in community structure and activity from the three further offshore stations in early winter and summer. Our data on the microbial community compositions and their seasonality support previous notions that the EMS behaves like an oceanic gyre.

Bioinformatics Service Unit University of Haifa Haifa Israel

Department of Aquatic Microbial Ecology Institute of Hydrobiology Biology Centre CAS České Budějovice Czechia

Department of Biological Oceanography Centro de Investigación Científica y de Educación Superior de Ensenada Ensenada Mexico

Department of Biological Sciences University of Southern California Los Angeles CA United States

Department of Marine Biology Leon H Charney School of Marine Sciences University of Haifa Haifa Israel

Morris Kahn Marine Research Station Environmental Geochemistry Lab Leon H Charney School of Marine Sciences University of Haifa Haifa Israel

The Dr Moses Strauss Department of Marine Geosciences Leon H Charney School of Marine Sciences University of Haifa Haifa Israel

Zobrazit více v PubMed

Alonso-Sáez L., Balagué V., Sà E. L., Sánchez O., González J. M., Pinhassi J., et al. . (2007). Seasonality in bacterial diversity in north-West Mediterranean coastal waters: assessment through clone libraries, fingerprinting and FISH. FEMS Microbiol. Ecol. 60, 98–112. doi: 10.1111/j.1574-6941.2006.00276.x, PMID: PubMed DOI

Armstrong F. A. J., Stearns C. R., Strickland J. D. H. (1967). The measurement of upwelling and subsequent biological process by means of the Technicon Autoanalyzer® and associated equipment. Deep-Sea Res. Oceanogr. Abstr. 14, 381–389. doi: 10.1016/0011-7471(67)90082-4 DOI

Auladell A., Barberán A., Logares R., Garcés E., Gasol J. M., Ferrera I. (2021). Seasonal niche differentiation among closely related marine bacteria. ISME J. 16, 178–189. doi: 10.1038/s41396-021-01053-2, PMID: PubMed DOI PMC

Ben Ezra T., Krom M. D., Tsemel A., Berman-Frank I., Herut B., Lehahn Y., et al. . (2021). Seasonal nutrient dynamics in the P depleted eastern Mediterranean Sea. Deep-Sea Res. I Oceanogr. Res. Pap. 176:103607. doi: 10.1016/j.dsr.2021.103607 DOI

Berman T., Azov Y., Schneller A., Walline P., Townsend D. (1986). Extent, transparency and phytoplankton distribution of the neritic waters overlying the Israeli coastal shelf. Oceanol. Acta 9, 439–447.

Bryant J. A., Aylward F. O., Eppley J. M., Karl D. M., Church M. J., DeLong E. F. (2016). Wind and sunlight shape microbial diversity in surface waters of the North Pacific subtropical gyre. ISME J. 10, 1308–1322. doi: 10.1038/ismej.2015.221, PMID: PubMed DOI PMC

Callahan B. J., McMurdie P. J., Rosen M. J., Han A. W., Johnson A. J. A., Holmes S. P. (2016). DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583. doi: 10.1038/nmeth.3869, PMID: PubMed DOI PMC

Camarena-Gómez M. T., Lipsewers T., Piiparinen J., Eronen-Rasimus E., Perez-Quemaliños D., Hoikkala L., et al. . (2018). Shifts in phytoplankton community structure modify bacterial production, abundance and community composition. Aquat. Microb. Ecol. 81, 149–170. doi: 10.3354/ame01868 DOI

Campbell B. J., Kirchman D. L. (2013). Bacterial diversity, community structure and potential growth rates along an estuarine salinity gradient. ISME J. 7, 210–220. doi: 10.1038/ismej.2012.93, PMID: PubMed DOI PMC

Campbell B. J., Yu L., Heidelberg J. F., Kirchman D. L. (2011). Activity of abundant and rare bacteria in a coastal ocean. PNAS 108, 12776–12781. doi: 10.1073/pnas.1101405108, PMID: PubMed DOI PMC

Carlson C. A., Morris R., Parsons R., Treusch A. H., Giovannoni S. J., Vergin K. (2009). Seasonal dynamics of SAR11 populations in the euphotic and mesopelagic zones of the northwestern Sargasso Sea. ISME J. 3, 283–295. doi: 10.1038/ismej.2008.117, PMID: PubMed DOI

D’Alimonte D., Zibordi G. (2003). Phytoplankton determination in an optically complex coastal region using a multilayer perceptron neural network. IEEE Trans. Geosc. Remote Sens. 41, 2861–2868. doi: 10.1109/tgrs.2003.817682 DOI

De Cáceres M., Legendre P., Moretti M. (2010). Improving indicator species analysis by combining groups of sites. Oikos 119, 1674–1684. doi: 10.1111/j.1600-0706.2010.18334.x DOI

Dubinsky V., Haber M., Burgsdorf I., Saurav K., Lehahn Y., Malik A., et al. . (2017). Metagenomic analysis reveals unusually high incidence of proteorhodopsin genes in the ultra-oligotrophic eastern Mediterranean Sea. Environ. Microbiol. 19, 1077–1090. doi: 10.1111/1462-2920.13624, PMID: PubMed DOI

Eiler A., Hayakawa D. H., Church M. J., Karl D. M., Rappé M. S. (2009). Dynamics of the SAR11 bacterioplankton lineage in relation to environmental conditions in the oligotrophic North Pacific subtropical gyre. Environ. Microbiol. 11, 2291–2300. doi: 10.1111/j.1462-2920.2009.01954.x, PMID: PubMed DOI

Falkowski P. G., Fenchel T., Delong E. F. (2008). The microbial engines that drive Earth’s biogeochemical cycles. Science 320, 1034–1039. doi: 10.1126/science.1153213, PMID: PubMed DOI

Feingersch R., Suzuki M. T., Shmoish M., Sharon I., Sabehi G., Partensky F., et al. . (2010). Microbial community genomics in eastern Mediterranean Sea surface waters. ISME J. 4, 78–87. doi: 10.1038/ismej.2009.92, PMID: PubMed DOI

Fortunato C. S., Herfort L., Zuber P., Baptista A. M., Crump B. C. (2011). Spatial variability overwhelms seasonal patterns in bacterioplankton communities across a river to ocean gradient. ISME J. 6, 554–563. doi: 10.1038/ismej.2011.135 PubMed DOI PMC

Fuhrman J. A., Cram J. A., Needham D. M. (2015). Marine microbial community dynamics and their ecological interpretation. Nat. Rev. Microbiol. 13, 133–146. doi: 10.1038/nrmicro3417, PMID: PubMed DOI

Fuhrman J. A., Hewson I., Schwalbach M. S., Steele J. A., Brown M. V., Naeem S. (2006). Annually reoccurring bacterial communities are predictable from ocean conditions. PNAS 103, 13104–13109. doi: 10.1073/pnas.0602399103, PMID: PubMed DOI PMC

Galand P. E., Pereira O., Hochart C., Auguet J. C., Debroas D. (2018). A strong link between marine microbial community composition and function challenges the idea of functional redundancy. ISME J. 12, 2470–2478. doi: 10.1038/s41396-018-0158-1, PMID: PubMed DOI PMC

Ghiglione J.-F., Larcher M., Lebaron P. (2005). Spatial and temporal scales of variation in bacterioplankton community structure in the NW Mediterranean Sea. Aquat. Microb. Ecol. 40, 229–240. doi: 10.3354/ame040229 DOI

Gilbert J. A., Steele J. A., Caporaso J. G., Steinbrück L., Reeder J., Temperton B., et al. . (2012). Defining seasonal marine microbial community dynamics. ISME J. 6, 298–308. doi: 10.1038/ismej.2011.107, PMID: PubMed DOI PMC

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

Grasshoff K., Ehrhardt M., Kremling K. (eds). (1983). Methods of Seawater Analysis: Second, Revised and Extended Edition. Verlag Chemie, Weihnheim, Germany.

Grasshoff K., Kremling K., Ehrhardt M. (eds). (2009). Methods of Seawater Analysis. John Wiley & Sons, Chichester.

Green S. J., Venkatramanan R., Naqib A. (2015). Deconstructing the polymerase chain reaction: understanding and correcting bias associated with primer degeneracies and primer-template mismatches. PLoS One 10:e0128122. doi: 10.1371/journal.pone.0128122 PubMed DOI PMC

Hammer O., Harper D., Ryan P. (2001). PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4:9.

Haro-Moreno J. M., Lopez-Perez M., de la Torre J. R., Picazo A., Camacho A., Rodriguez-Valera F. (2018). Fine metagenomic profile of the Mediterranean stratified and mixed water columns revealed by assembly and recruitment. Microbiome 6:128. doi: 10.1186/s40168-018-0513-5, PMID: PubMed DOI PMC

Hazan O., Silverman J., Sisma-Ventura G., Ozer T., Gertman I., Shoham-Frider E., et al. . (2018). Mesopelagic prokaryotes alter surface phytoplankton production during simulated deep mixing experiments in eastern Mediterranean Sea waters. Front. Mar. Sci. 5:1. doi: 10.3389/fmars.2018.00001 PubMed DOI

Hoarfrost A., Neyfach S., Ladau J., Yooseph S., Arnosti S., Dupont C. L., et al. . (2020). Global ecotypes in the ubiquitous marine clade SAR86. ISME J. 14, 178–188. doi: 10.1038/s41396-019-0516-7, PMID: PubMed DOI PMC

Kérouel R., Aminot A. (1997). Fluorometric determination of ammonia in sea and estuarine waters by direct segmented flow analysis. Mar. Chem. 57, 265–275. doi: 10.1016/s0304-4203(97)00040-6 DOI

Keuter S., Rahav E., Herut B., Rinkevich B. (2015). Distribution patterns of bacterioplankton in the oligotrophic South-Eastern Mediterranean Sea. FEMS Microbiol. Ecol. 91:fiv070. doi: 10.1093/femsec/fiv070, PMID: PubMed DOI

Korlević M., Pop Ristova P., Garić R., Amann R., Orlić S. (2015). Bacterial diversity in the South Adriatic Sea during a strong, deep winter convection year. Appl. Environ. Microbiol. 81, 1715–1726. doi: 10.1128/AEM.03410-14, PMID: PubMed DOI PMC

Kress N., Herut B. (2001). Spatial and seasonal evolution of dissolved oxygen and nutrients in the Southern Levantine Basin (Eastern Mediterranean Sea): chemical characterization of the water masses and inferences on the N:P ratios. Deep-Sea Res. I Oceanogr. Res. Pap. 48, 2347–2372. doi: 10.1016/s0967-0637(01)00022-x DOI

Krom M. D., Emeis K.-C., Cappellen P. V. (2010). Why is the eastern Mediterranean phosphorus limited? Prog. Oceanogr. 85, 236–244. doi: 10.1016/j.pocean.2010.03.003 DOI

Krom M., Kress N., Berman-Frank I., Rahav E. (2014). “Past, present and future patterns in the nutrient chemistry of the Eastern Mediterranean,” in The Mediterranean Sea: Its History and Present Challenges. eds. Goffredo S., Dubinsky Z. (Netherlands: Springer; ), 49–68.

Krom M. D., Kress N., Brenner S., Gordon L. I. (1991). Phosphorus limitation of primary productivity in the eastern Mediterranean Sea. Limnol. Oceanogr. 36, 424–432. doi: 10.4319/lo.1991.36.3.0424 DOI

Krom M. D., Woodward E. M. S., Herut B., Kress N., Carbo P., Mantoura R. F. C., et al. . (2005). Nutrient cycling in the southeast Levantine basin of the eastern Mediterranean: results from a phosphorus starved system. Deep-Sea Res. II Top. Stud. Oceanogr. 52, 2879–2896. doi: 10.1016/j.dsr2.2005.08.009 DOI

Lehahn Y., Koren I., Sharoni S., d’Ovidio F., Vardi A., Boss E. (2017). Dispersion/dilution enhances phytoplankton blooms in low-nutrient waters. Nat. Commun. 8:14868. doi: 10.1038/ncomms14868, PMID: PubMed DOI PMC

Lucas J., Wichels A., Gerdts G. (2016). Spatiotemporal variation of the bacterioplankton community in the German bight: from estuarine to offshore regions. Helgol. Mar. Res. 70:16. doi: 10.1186/s10152-016-0464-9 DOI

Magoč T., Salzberg S. L. (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963. doi: 10.1093/bioinformatics/btr507, PMID: PubMed DOI PMC

Mella-Flores D., Six C., Ratin M., Partensky F., Boutte C., Le Corguillé G., et al. . (2012). Prochlorococcus and Synechococcus have evolved different adaptive mechanisms to cope with light and UV stress. Front. Microbiol. 3:285. doi: 10.3389/fmicb.2012.00285, PMID: PubMed DOI PMC

Mestre M., Borrull E., Sala M. M., Gasol J. M. (2017). Patterns of bacterial diversity in the marine planktonic particulate matter continuum. ISME J. 11, 999–1010. doi: 10.1038/ismej.2016.166, PMID: PubMed DOI PMC

Moonsamy P. V., Williams T., Bonella P., Holcomb C. L., Höglund B. N., Hillman G., et al. . (2013). High throughput HLA genotyping using 454 sequencing and the Fluidigm access Array™ system for simplified amplicon library preparation: high throughput HLA 454 sequencing using the Fluidigm access Array™ system. Tissue Antigens 81, 141–149. doi: 10.1111/tan.12071, PMID: PubMed DOI

Morales S. E., Meyer M., Currie K., Baltar F. (2018). Are oceanic fronts ecotones? Seasonal changes along the subtropical front show fronts as bacterioplankton transition zones but not diversity hotspots. Environ. Microbiol. Rep. 10, 184–189. doi: 10.1111/1758-2229.12618, PMID: PubMed DOI

Morris R. M., Frazar C. D., Carlson C. A. (2012). Basin-scale patterns in the abundance of SAR11 subclades, marine Actinobacteria (OM1), members of the Roseobacter clade and OCS116 in the South Atlantic. Environ. Microbiol. 14, 1133–1144. doi: 10.1111/j.1462-2920.2011.02694.x, PMID: PubMed DOI

Murphy J., Riley J. P. (1962). A modified single solution method for the determination of phosphate in natural waters. Anal. Chim. Acta 27, 31–36. doi: 10.1016/S0003-2670(00)88444-5, PMID: PubMed DOI

Oksanen J., Blanchet F. G., Friendly M., Kindt R., Legendre P., McGlinn D., et al. . (2017). Vegan: Community Ecology Package version 2.5-7. Available at: https://CRAN.R-project.org/package=vegan

Parada A. E., Needham D. M., Fuhrman J. A. (2016). Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18, 1403–1414. doi: 10.1111/1462-2920.13023, PMID: PubMed DOI

Powley H. R., Krom M. D., Cappellen P. V. (2017). Understanding the unique biogeochemistry of the Mediterranean Sea: insights from a coupled phosphorus and nitrogen model: P and N cycling in the Mediterranean Sea. Glob. Biogeochem. Cycles 31, 1010–1031. doi: 10.1002/2017gb005648 DOI

Quéméneur M., Bel Hassen M., Armougom F., Khammeri Y., Lajnef R., Bellaaj-Zouari A. (2020). Prokaryotic diversity and distribution along physical and nutrient gradients in the Tunisian coastal waters (South Mediterranean Sea). Front. Microbiol. 11:593540. doi: 10.3389/fmicb.2020.593540, PMID: PubMed DOI PMC

Quero G. M., Luna G. M. (2014). Diversity of rare and abundant bacteria in surface waters of the southern Adriatic Sea. Mar. Genomics 17, 9–15. doi: 10.1016/j.margen.2014.04.002, PMID: PubMed DOI

Raveh O., David N., Rilov G., Rahav E. (2015). The temporal dynamics of coastal phytoplankton and bacterioplankton in the eastern Mediterranean Sea. PLoS One 10:e0140690. doi: 10.1371/journal.pone.0140690, PMID: PubMed DOI PMC

Reich T., Ben-Ezra T., Belkin N., Tsemel A., Aharonovich D., Roth-Rosenberg D., et al. . (2021). Seasonal dynamics of phytoplankton and bacterioplankton at the ultra-oligotrophic southeastern Mediterranean Sea. Deep Sea Res. I: Oceanogr. Res. Pap. 182:103720. doi: 10.1016/j.dsr.2022.103720 DOI

Roth Rosenberg D., Haber M., Goldford J., Lalzar M., Aharonovich D., Al-Ashhab A., et al. . (2021). Particle-associated and free-living bacterial communities in an oligotrophic sea are affected by different environmental factors. Environ. Microbiol. 23, 4295–4308. doi: 10.1111/1462-2920.15611, PMID: PubMed DOI

Salter I., Galand P. E., Fagervold S. K., Lebaron P., Obernosterer I., Oliver M. J., et al. . (2015). Seasonal dynamics of active SAR11 ecotypes in the oligotrophic Northwest Mediterranean Sea. ISME J. 9, 347–360. doi: 10.1038/ismej.2014.129, PMID: PubMed DOI PMC

Schlitzer R. (2015). Data analysis and visualization with Ocean Data View. CMOS Bulletin SCM. 43, 9–13. doi: 10013/epic.45187.d001

Schloss P. D., Westcott S. L., Ryabin T., Hall J. R., Hartmann M., Hollister E. B., et al. . (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541. doi: 10.1128/AEM.01541-09 PubMed DOI PMC

Sebastián M., Ortega-Retuerta E., Gómez-Consarnau L., Zamanillo M., Álvarez M., Arístegui J., et al. . (2021). Environmental gradients and physical barriers drive the basin-wide spatial structuring of Mediterranean Sea and adjacent eastern Atlantic Ocean prokaryotic communities. Limnol. Oceanogr. 66, 4077–4095. doi: 10.1002/lno.11944 DOI

Smyth T. J. (2011). Penetration of UV irradiance into the global ocean. J. Geophys. Res. 116:C11020. doi: 10.1029/2011jc007183 DOI

Sunagawa S., Coelho L. P., Chaffron S., Kultima J. R., Labadie K., Salazar G., et al. . (2015). Ocean plankton. Structure and function of the global ocean microbiome. Science 348:1261359. doi: 10.1126/science.1261359 PubMed DOI

Tanaka T., Thingstad T. F., Christaki U., Colombet J., Cornet-Barthaux V., Courties C., et al. . (2011). Lack of P-limitation of phytoplankton and heterotrophic prokaryotes in surface waters of three anticyclonic eddies in the stratified Mediterranean Sea. Biogeosciences 8, 525–538. doi: 10.5194/bg-8-525-2011 DOI

Tedetti M., Sempéré R. (2006). Penetration of ultraviolet radiation in the marine environment: a review. Photochem. Photobiol. 82, 389–397. doi: 10.1562/2005-11-09-IR-733, PMID: PubMed DOI

Thingstad T. F., Krom M. D., Mantoura R. F. C., Flaten G. A. F., Groom S., Herut B., et al. . (2005). Nature of phosphorus limitation in the ultra-oligotrophic eastern Mediterranean. Science 309, 1068–1071. doi: 10.1126/science.1112632, PMID: PubMed DOI

Tinta T., Vojvoda J., Mozetič P., Talaber I., Vodopivec M., Malfatti F., et al. . (2015). Bacterial community shift is induced by dynamic environmental parameters in a changing coastal ecosystem (northern Adriatic, northeastern Mediterranean Sea): a 2-year time-series study: bacterial community shift in a dynamic coastal ecosystem. Environ. Microbiol. 17, 3581–3596. doi: 10.1111/1462-2920.12519, PMID: PubMed DOI

Tsiola A., Pitta P., Fodelianakis S., Pete R., Magiopoulos I., Mara P., et al. . (2016). Nutrient limitation in surface waters of the oligotrophic eastern Mediterranean Sea: an enrichment microcosm experiment. Microb. Ecol. 71, 575–588. doi: 10.1007/s00248-015-0713-5, PMID: PubMed DOI

Vergin K. L., Beszteri B., Monier A., Thrash J. C., Temperton B., Treusch A. H., et al. . (2013). High-resolution SAR11 ecotype dynamics at the Bermuda Atlantic time-series study site by phylogenetic placement of pyrosequences. ISME J. 7:1322. doi: 10.1038/ismej.2013.32, PMID: PubMed DOI PMC

Volpe G., Santoleri R., Vellucci V., d’Alcalà M. R., Marullo S., D’Ortenzio F. (2007). The colour of the Mediterranean Sea: global versus regional bio-optical algorithms evaluation and implication for satellite chlorophyll estimates. Remote Sens. Environ. 107, 625–638. doi: 10.1016/j.rse.2006.10.017 DOI

Wang Z., Juarez D. L., Pan J.-F., Blinebry S. K., Gronniger J., Clark J. S., et al. . (2019). Microbial communities across nearshore to offshore coastal transects are primarily shaped by distance and temperature. Environ. Microbiol. 21, 3862–3872. doi: 10.1111/1462-2920.14734, PMID: PubMed DOI

Ward C. S., Yung C.-M., Davis K. M., Blinebry S. K., Williams T. C., Johnson Z. I., et al. . (2017). Annual community patterns are driven by seasonal switching between closely related marine bacteria. ISME J. 11, 1412–1422. doi: 10.1038/ismej.2017.4, PMID: PubMed DOI PMC

West N. J., Lepère C., de Manes C.-L., Catala P., Scanlan D. J., Lebaron P. (2016). Distinct spatial patterns of SAR11, SAR86, and Actinobacteria diversity along a transect in the ultra-oligotrophic South Pacific Ocean. Front. Microbiol. 7:234. doi: 10.3389/fmicb.2016.00234, PMID: PubMed DOI PMC

Rhodopsin-mediated nutrient uptake by cultivated photoheterotrophic Verrucomicrobiota