Environmental stability impacts the differential sensitivity of marine microbiomes to increases in temperature and acidity


Ambient conditions shape microbiome responses to both short- and long-duration environment changes through processes including physiological acclimation, compositional shifts, and evolution. Thus, we predict that microbial communities inhabiting locations with larger diel, episodic, and annual variability in temperature and pH should be less sensitive to shifts in these climate-change factors. To test this hypothesis, we compared responses of surface ocean microbes from more variable (nearshore) and more constant (offshore) sites to short-term factorial warming (+3 °C) and/or acidification (pH −0.3). In all cases, warming alone significantly altered microbial community composition, while acidification had a minor influence. Compared with nearshore microbes, warmed offshore microbiomes exhibited larger changes in community composition, phylotype abundances, respiration rates, and metatranscriptomes, suggesting increased sensitivity of microbes from the less-variable environment. Moreover, while warming increased respiration rates, offshore metatranscriptomes yielded evidence of thermal stress responses in protein synthesis, heat shock proteins, and regulation. Future oceans with warmer waters may enhance overall metabolic and biogeochemical rates, but they will host altered microbial communities, especially in relatively thermally stable regions of the oceans.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: Nonmetric multidimensional scaling (NMDS) ordination computed based on Bray–Curtis dissimilarity for 16S rRNA gene libraries.
Fig. 2: Phylotypes (ASVs) that significantly respond to warming.
Fig. 3: Log2 fold changes of SEED subsystems in response to warming in two experiments (nearshore winter and offshore winter).


  1. 1.

    Hutchins DA, Fu F. Microorganisms and ocean global change. Nat Microbiol. 2017;2:17058.

    CAS  PubMed  Google Scholar 

  2. 2.

    Shade A, Peter H, Allison SD, Baho DL, Berga M, Bürgmann H, et al. Fundamentals of microbial community resistance and resilience. Front Microbiol. 2012;3:417.

    PubMed  PubMed Central  Google Scholar 

  3. 3.

    Allison SD, Martiny JBH. Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci USA. 2008;105:11512–9.

    CAS  Google Scholar 

  4. 4.

    Eppley RW. Temperature and phytoplankton growth in the sea. Fish Bull. 1972;70:1063–85.

    Google Scholar 

  5. 5.

    Hawkes CV, Keitt TH. Resilience vs. historical contingency in microbial responses to environmental change. Ecol Lett. 2015;18:612–25.

    PubMed  Google Scholar 

  6. 6.

    Stegen JC, Bottos EM, Jansson JK. A unified conceptual framework for prediction and control of microbiomes. Curr Opin Microbiol. 2018;44:20–7.

    PubMed  Google Scholar 

  7. 7.

    Kling JD, Lee MD, Fu F, Phan MD, Wang X, Qu P, et al. Transient exposure to novel high temperatures reshapes coastal phytoplankton communities. ISME J. 2020;14:413–24.

    CAS  PubMed  Google Scholar 

  8. 8.

    Izem R, Kingsolver JG. Variation in continuous reaction norms: quantifying directions of biological interest. Am Naturalist. 2005;166:277–89.

    Google Scholar 

  9. 9.

    Thomas MK, Kremer CT, Klausmeier CA, Litchman E. A global pattern of thermal adaptation in marine phytoplankton. Science. 2012;338:1085–8.

    CAS  PubMed  Google Scholar 

  10. 10.

    Lomas M, Hopkinson B, Ryan JLD, Shi D, Xu Y, Morel F. Effect of ocean acidification on cyanobacteria in the subtropical North Atlantic. Aquat Microb Ecol. 2012;66:211–22.

    Google Scholar 

  11. 11.

    Dutkiewicz S, Morris JJ, Follows MJ, Scott J, Levitan O, Dyhrman ST, et al. Impact of ocean acidification on the structure of future phytoplankton communities. Nat Clim Change. 2015;5:1002–6.

    CAS  Google Scholar 

  12. 12.

    Hunt DE, Ward CS. A network-based approach to disturbance transmission through microbial interactions. Front Microbiol. 2015;6:1182. http://www.frontiersin.org/Journal/Abstract.aspx?s=53&name=aquatic_microbiology&ART_DOI=10.3389/fmicb.2015.01182.

  13. 13.

    Hennon GM, Morris JJ, Haley ST, Zinser ER, Durrant AR, Entwistle E, et al. The impact of elevated CO2 on Prochlorococcus and microbial interactions with ‘helper’ bacterium Alteromonas. The ISME J. 2017;12:520–31.

    Google Scholar 

  14. 14.

    von Scheibner M, Dörge P, Biermann A, Sommer U, Hoppe HG, Jürgens K. Impact of warming on phyto‐bacterioplankton coupling and bacterial community composition in experimental mesocosms. Environ Microbiol. 2014;16:718–33.

    Google Scholar 

  15. 15.

    Toseland A, Daines SJ, Clark JR, Kirkham A, Strauss J, Uhlig C, et al. The impact of temperature on marine phytoplankton resource allocation and metabolism. Nat Clim Change. 2013;3:979–84.

    CAS  Google Scholar 

  16. 16.

    Ward CS, Yung C-M, Davis KM, Blinebry SK, Williams TC, Johnson ZI, et al. Annual community patterns are driven by seasonal switching between closely related marine bacteria. ISME J. 2017;11:1412–22.

    PubMed  PubMed Central  Google Scholar 

  17. 17.

    Johnson ZI, Zinser ER, Coe A, McNulty NP, Woodward EMS, Chisholm SW. Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science. 2006;311:1737–40.

    CAS  PubMed  Google Scholar 

  18. 18.

    Fuhrman JA, Steele JA, Hewson I, Schwalbach MS, Brown MV, Green JL, et al. A latitudinal diversity gradient in planktonic marine bacteria. Proc Natl Acad Sci USA. 2008;105:7774–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Doo SS, Kealoha A, Andersson A, Cohen AL, Hicks TL, Johnson ZI, et al. The challenges of detecting and attributing ocean acidification impacts on marine ecosystems. ICES J Mar Sci. 2020. https://doi.org/10.1093/icesjms/fsaa094.

  20. 20.

    Lindh MV, Riemann L, Baltar F, Romero‐Oliva C, Salomon PS, Granéli E, et al. Consequences of increased temperature and acidification on bacterioplankton community composition during a mesocosm spring bloom in the Baltic Sea. Environ Microbiol Rep. 2013;5:252–62.

    CAS  PubMed  Google Scholar 

  21. 21.

    Roy A-S, Gibbons S, Schunck H, Owens S, Caporaso J, Sperling M, et al. Ocean acidification shows negligible impacts on high-latitude bacterial community structure in coastal pelagic mesocosms. Biogeosciences. 2013;10:555–66.

    Google Scholar 

  22. 22.

    Oliver AE, Newbold LK, Whiteley AS, van der Gast CJ. Marine bacterial communities are resistant to elevated carbon dioxide levels. Environ Microbiol Rep. 2014;6:574–82.

    CAS  PubMed  Google Scholar 

  23. 23.

    Newbold LK, Oliver AE, Booth T, Tiwari B, DeSantis T, Maguire M, et al. The response of marine picoplankton to ocean acidification. Environ Microbiol. 2012;14:2293–307.

    CAS  PubMed  Google Scholar 

  24. 24.

    Bergen B, Endres S, Engel A, Zark M, Dittmar T, Sommer U, et al. Acidification and warming affect prominent bacteria in two seasonal phytoplankton bloom mesocosms. Environ Microbiol. 2016;18:4579–95.

    CAS  PubMed  Google Scholar 

  25. 25.

    Bunse C, Lundin D, Karlsson CM, Akram N, Vila-Costa M, Palovaara J, et al. Response of marine bacterioplankton pH homeostasis gene expression to elevated CO2. Nat Clim Change. 2016;6:483–7.

    CAS  Google Scholar 

  26. 26.

    Xia X, Wang Y, Yang Y, Luo T, Van Nostrand JD, Zhou J, et al. Ocean acidification regulates the activity, community structure, and functional potential of heterotrophic bacterioplankton in an oligotrophic gyre. J Geophys Res. 2019;124:1001–17.

    CAS  Google Scholar 

  27. 27.

    Crawfurd KJ, Alvarez-Fernandez S, Mojica KD, Riebesell U, Brussaard CP. Alterations in microbial community composition with increasing fCO2: a mesocosm study in the eastern Baltic Sea. Biogeosciences. 2017;14:3831–49.

    CAS  Google Scholar 

  28. 28.

    Johnson ZI, Wheeler BJ, Blinebry SK, Carlson CM, Ward CS, Hunt DE. Dramatic variability of the carbonate system at a temperate coastal ocean site (Beaufort, North Carolina, USA) is regulated by physical and biogeochemical processes on multiple timescales. PLoS ONE. 2013;8:e85117.

    PubMed  PubMed Central  Google Scholar 

  29. 29.

    Wang Z, Juarez DL, Pan JF, Blinebry SK, Gronniger J, Clark JS, et al. Microbial communities across nearshore to offshore coastal transects are primarily shaped by distance and temperature. Environ Microbiol. 2019;21:3862–72.

    CAS  PubMed  Google Scholar 

  30. 30.

    Dore JE, Lukas R, Sadler DW, Church MJ, Karl DM. Physical and biogeochemical modulation of ocean acidification in the central North Pacific. Proc Natl Acad Sci USA. 2009;106:12235–40.

    CAS  PubMed  Google Scholar 

  31. 31.

    Giovannoni SJ, Thrash JC, Temperton B. Implications of streamlining theory for microbial ecology. ISME J. 2014;8:1553–65.

    PubMed  PubMed Central  Google Scholar 

  32. 32.

    Caldeira K, Wickett ME. Anthropogenic carbon and ocean pH. Nature. 2003;425:365.

    CAS  PubMed  Google Scholar 

  33. 33.

    Clayton TD, Byrne RH. Spectrophotometric seawater pH measurements: total hydrogen ion concentration scale calibration of m-cresol purple and at-sea results. Deep Sea Res Part I. 1993;40:2115–29.

    CAS  Google Scholar 

  34. 34.

    Barber RT, Marra J, Bidigare RC, Codispoti LA, Halpern D, Johnson Z, et al. Primary productivity and its regulation in the Arabian Sea during 1995. Deep Sea Res Part II. 2001;48:1127–72.

    CAS  Google Scholar 

  35. 35.

    Labasque T, Chaumery C, Aminot A, Kergoat G. Spectrophotometric Winkler determination of dissolved oxygen: re-examination of critical factors and reliability. Marine Chemistry. 2004;88:53–60.

  36. 36.

    Johnson ZI, Shyam R, Ritchie AE, Mioni C, Lance VP, Murray JW, et al. The effect of iron-and light-limitation on phytoplankton communities of deep chlorophyll maxima of the western Pacific Ocean. J Mar Res. 2010;68:283–308.

    CAS  Google Scholar 

  37. 37.

    Marie D, Partensky F, Jacquet S, Vaulot D. Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I. Appl Environ Microbiol. 1997;63:186–93.

    CAS  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol. 2016;18:1403–14.

    CAS  PubMed  Google Scholar 

  39. 39.

    Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996–8.

    CAS  PubMed  Google Scholar 

  40. 40.

    Eren AM, Morrison HG, Lescault PJ, Reveillaud J, Vineis JH, Sogin ML. Minimum entropy decomposition: unsupervised oligotyping for sensitive partitioning of high-throughput marker gene sequences. ISME J. 2015;9:968–79.

    CAS  PubMed  Google Scholar 

  41. 41.

    Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara R, et al. Package ‘vegan’. Community ecology package, version. 2015;2.

  42. 42.

    Tsementzi D, Poretsky R, Rodriguez-R LM, Luo C, Konstantinidis KT. Evaluation of metatranscriptomic protocols and application to the study of freshwater microbial communities. Environ Microbiol Rep. 2014;6:640–55.

    CAS  PubMed  Google Scholar 

  43. 43.

    Cox MP, Peterson DA, Biggs PJ. SolexaQA: at-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinform. 2010;11:485.

    Google Scholar 

  44. 44.

    Bengtsson‐Palme J, Hartmann M, Eriksson KM, Pal C, Thorell K, Larsson DGJ, et al. METAXA2: improved identification and taxonomic classification of small and large subunit rRNA in metagenomic data. Mol Ecol Resour. 2015;15:1403–14.

    PubMed  Google Scholar 

  45. 45.

    Kopylova E, Noé L, Touzet H. SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics. 2012;28:3211–7.

    CAS  PubMed  Google Scholar 

  46. 46.

    Burge SW, Daub J, Eberhardt R, Tate J, Barquist L, Nawrocki EP, et al. Rfam 11.0: 10 years of RNA families. Nucleic Acids Res. 2012;41:D226–32.

    PubMed  PubMed Central  Google Scholar 

  47. 47.

    Kent WJ. BLAT—the BLAST-like alignment tool. Genome Res. 2002;12:656–64.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Parks DH, Rinke C, Chuvochina M, Chaumeil P-A, Woodcroft BJ, Evans PN, et al. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat Microbiol. 2017;2:1533–42.

    CAS  PubMed  Google Scholar 

  49. 49.

    Tully BJ, Graham ED, Heidelberg JF. The reconstruction of 2,631 draft metagenome-assembled genomes from the global oceans. Sci data. 2018;5:170203.

    CAS  PubMed  PubMed Central  Google Scholar 

  50. 50.

    Rodriguez-R LM, Tsementzi D, Luo C, Konstantinidis KT. Iterative subtractive binning of freshwater chronoseries metagenomes identifies over 400 novel species and their ecologic preferences. Environ Microbiol. 2020;22:3394–412.

    CAS  PubMed  Google Scholar 

  51. 51.

    Tsementzi D, Rodriguez-R LM, Ruiz-Perez CA, Meziti A, Hatt JK, Konstantinidis KT. Ecogenomic characterization of widespread, closely-related SAR11 clades of the freshwater genus “Candidatus Fonsibacter” and proposal of Ca. Fonsibacter lacus sp. nov. Syst Appl Microbiol. 2019;42:495–505.

    PubMed  Google Scholar 

  52. 52.

    Wu CH, Apweiler R, Bairoch A, Natale DA, Barker WC, Boeckmann B, et al. The universal protein resource (UniProt): an expanding universe of protein information. Nucleic Acids Res. 2006;34:D187–91.

    CAS  PubMed  Google Scholar 

  53. 53.

    Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology: tool for the unification of biology. Nat Genet. 2000;25–29:25.

    Google Scholar 

  54. 54.

    Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang H-Y, Cohoon M, et al. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res. 2005;33:5691–702.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. 55.

    Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12:59.

    CAS  PubMed  Google Scholar 

  56. 56.

    Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:1.

    Google Scholar 

  57. 57.

    Wohlers J, Engel A, Zöllner E, Breithaupt P, Jürgens K, Hoppe HG, et al. Changes in biogenic carbon flow in response to sea surface warming. Proc Natl Acad Sci USA. 2009;106:7067–72.

    CAS  PubMed  Google Scholar 

  58. 58.

    Fu F-X, Warner ME, Zhang Y, Feng Y, Hutchins DA. Effects of increased temperature and CO2 on photosynthesis, growth, and elemental rations in marine Synechoccocus and Prochlorococcus (Cyanobacteria). J Phycol. 2007;43:485–96.

    Google Scholar 

  59. 59.

    Riebesell U, Wolf-Gladrow D, Smetacek V. Carbon dioxide limitation of marine phytoplankton growth rates. Nature. 1993;361:249–51.

    CAS  Google Scholar 

  60. 60.

    McCarthy A, Rogers SP, Duffy SJ, Campbell DA. Elevated carbon dioxide differentially alters the photophysiology of Thalassiosira pseudonana (Bacillariophyceae) and Emiliania huxleyi (Haptophyta). J Phycol. 2012;48:635–46.

    CAS  PubMed  Google Scholar 

  61. 61.

    Fuhrman JA, Hewson I, Schwalbach MS, Steele JA, Brown MV, Naeem S. Annually reoccurring bacterial communities are predictable from ocean conditions. Proc Natl Acad Sci USA. 2006;103:13104–9.

    CAS  PubMed  Google Scholar 

  62. 62.

    Baltar F, Palovaara J, Vila-Costa M, Salazar G, Calvo E, Pelejero C, et al. Response of rare, common and abundant bacterioplankton to anthropogenic perturbations in a Mediterranean coastal site. FEMS Microbiol Ecol. 2015;91:fiv058.

    PubMed  Google Scholar 

  63. 63.

    Paerl HW, Huisman J. Blooms like it hot. Science. 2008;320:57–8.

    CAS  PubMed  Google Scholar 

  64. 64.

    Yung C-M, Vereen MK, Herbert A, Davis KM, Yang J, Kantorowska A, et al. Thermally adaptive tradeoffs in closely-related marine bacterial strains. Environ Microbiol. 2015;17:2421–9.

    PubMed  Google Scholar 

  65. 65.

    Gao H, Wang Y, Liu X, Yan T, Wu L, Alm E, et al. Global transcriptome analysis of the heat shock response of Shewanella oneidensis. J Bacteriol. 2004;186:7796–803.

    CAS  PubMed  PubMed Central  Google Scholar 

  66. 66.

    van der Veen S, Hain T, Wouters JA, Hossain H, de Vos WM, Abee T, et al. The heat-shock response of Listeria monocytogenes comprises genes involved in heat shock, cell division, cell wall synthesis, and the SOS response. Microbiology. 2007;153:3593–607.

    PubMed  Google Scholar 

  67. 67.

    Hall EK, Singer GA, Kainz MJ, Lennon JT. Evidence for a temperature acclimation mechanism in bacteria: an empirical test of a membrane-mediated trade-off. Funct Ecol. 2010;24:898–908.

    Google Scholar 

  68. 68.

    Lauro FM, McDougald D, Thomas T, Williams TJ, Egan S, Rice S, et al. The genomic basis of trophic strategy in marine bacteria. Proc Natl Acad Sci USA. 2009;106:15527–33.

    CAS  PubMed  Google Scholar 

  69. 69.

    Yutin N, Puigbò P, Koonin EV, Wolf YI. Phylogenomics of prokaryotic ribosomal proteins. PLoS ONE. 2012;7:5.

    Google Scholar 

  70. 70.

    Blazewicz SJ, Barnard RL, Daly RA, Firestone MK. Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses. ISME J. 2013;7:2061–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  71. 71.

    Hunt DE, Lin Y, Church MJ, Karl DM, Izzo LK, Tringe S, et al. Relationship between abundance and specific activity of bacterioplankton in open ocean surface waters. Appl Environ Microbiol. 2013;79:177–84.

    CAS  PubMed  PubMed Central  Google Scholar 

  72. 72.

    Boeuf D, Edwards BR, Eppley JM, Hu SK, Poff KE, Romano AE, et al. Biological composition and microbial dynamics of sinking particulate organic matter at abyssal depths in the oligotrophic open ocean. Proc Natl Acad Sci USA. 2019;116:11824–32.

    CAS  PubMed  Google Scholar 

Download references


We acknowledge the contribution of the entire PICO sampling team to field work. We specifically acknowledge funding from the Moore Foundation to DEH (GBMF3768) and the National Science Foundation to DEH and ZIJ (OCE:1416665) and KTK (OCE:1416673).

Author information



Corresponding author

Correspondence to Dana E. Hunt.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wang, Z., Tsementzi, D., Williams, T.C. et al. Environmental stability impacts the differential sensitivity of marine microbiomes to increases in temperature and acidity. ISME J (2020). https://doi.org/10.1038/s41396-020-00748-2

Download citation