Decoupling of bacterial production and respiration in the surface water of the North Pacific Subtropical Gyre

Yuchen Zhang , Yibin Huang , Feipeng Xu , Shujie Cai , Yao Liu , Chao Xu , Lizhen Lin , Jixin Chen , Edward Allen Laws , Xin Liu , Bangqin Huang

Marine Life Science & Technology ›› 2025, Vol. 7 ›› Issue (2) : 397 -412.

PDF
Marine Life Science & Technology ›› 2025, Vol. 7 ›› Issue (2) : 397 -412. DOI: 10.1007/s42995-025-00279-9
Research Paper

Decoupling of bacterial production and respiration in the surface water of the North Pacific Subtropical Gyre

Author information +
History +
PDF

Abstract

Heterotrophic bacterial production and respiration, two important contributors to carbon cycling, play an important role in global biogeochemical cycles. However, recent research suggests that these two processes may be decoupled, and the underlying changes in community structure and their interactions remain unclear. In this study, two research expeditions to the North Pacific Subtropical Gyre (NPSG) during the summer and winter of 2020–2021 revealed seasonal shifts in bacterial metabolism and community structure in response to environmental factors. The findings indicated notable seasonal fluctuations in bacterial abundance and production in the surface waters. Both peaked in winter compared to summer. Alterations in bacterial abundance that were further evident at the community level demonstrated significant seasonal differences in bacterial community structure and diversity and revealed, in particular, the intricacy of the networks and interactions among bacterial communities in winter. Bacterial respiration displayed no significant seasonal variations and was decoupled from bacterial abundance and production. The implication was that bacterial production did not directly dictate bacterial respiration. Specific taxa exerted a more substantial influence on bacterial respiration, potentially including groups with high respiration rates but relatively low abundance, thus challenging the notion that highly abundant taxa are invariably the most metabolically active. Moreover, the interplay between different bacterial taxa and their interactions may also impact the overall strength of bacterial community respiration. These findings significantly enhance our understanding of the decoupling between bacterial production and respiration, which is crucial for unraveling the complex mechanisms underlying carbon cycling and energy flow in marine ecosystems.

Keywords

Bacterial metabolism / Bacterial production / Bacterial respiration / Community structure / Subtropical gyre / Biological Sciences / Microbiology

Cite this article

Download citation ▾
Yuchen Zhang, Yibin Huang, Feipeng Xu, Shujie Cai, Yao Liu, Chao Xu, Lizhen Lin, Jixin Chen, Edward Allen Laws, Xin Liu, Bangqin Huang. Decoupling of bacterial production and respiration in the surface water of the North Pacific Subtropical Gyre. Marine Life Science & Technology, 2025, 7(2): 397-412 DOI:10.1007/s42995-025-00279-9

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

AzamF, MalfattiF. Microbial structuring of marine ecosystems. Nat Rev Microbiol, 2007, 5: 782-791.

[2]

AzamF, FenchelT, FieldJG, GrayJS, Meyer-ReilLA, ThingstadF. The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser, 1983, 10: 257-263.

[3]

BarberánA, BatesST, CasamayorEO, FiererN. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J, 2012, 6: 343-351.

[4]

BenjaminiY, KriegerAM, YekutieliD. Adaptive linear step-up procedures that control the false discovery rate. Biometrika, 2006, 93: 491-507.

[5]

BermanT, Holm-HansenO. Release of photoassimilated carbon as dissolved organic matter by marine phytoplankton. Mar Biol, 1974, 28: 305-310.

[6]

BolyenE, RideoutJR, DillonMR, BokulichNA, AbnetC, Al-GhalithGA, CaporasoJG. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol, 2019, 37: 852-857.

[7]

BouvierT, Del GiorgioPA, GasolJM. A comparative study of the cytometric characteristics of high and low nucleic-acid bacterioplankton cells from different aquatic ecosystems. Environ Microbiol, 2007, 9: 2050-2066.

[8]

BoydPW, ClaustreH, LevyM, SiegelDA, WeberT. Multi-faceted particle pumps drive carbon sequestration in the ocean. Nat, 2015, 520: 529-535

[9]

Boyer TP, García HE, Locarnini RA, Zweng MM, Mishonov AV, Reagan JR, Weathers KA, Baranova OK, Paver CR, Seidov D, Smolyar IV (2018) World ocean atlas. NOAA National Centers for Environmental Information. https://www.ncei.noaa.gov/archive/accession/NCEI-WOA18

[10]

CallahanBJ, McMurdiePJ, RosenMJ, HanAW, JohnsonAJ, HolmesSP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods, 2016, 13: 581-583.

[11]

CarlsonCA, GiovannoniSJ, HansellDA, GoldbergSJ, ParsonsR, OteroMP, WheelerBR. Effect of nutrient amendments on bacterioplankton production, community structure, and DOC utilization in the northwestern Sargasso Sea. Aquat Microb Ecol, 2002, 30: 19-36.

[12]

CarlsonCA, Del GiorgioPA, HerndlGJ. Microbes and the dissipation of energy and respiration: from cells to ecosystems. Oceanogr, 2007, 20: 89-100.

[13]

CarlsonCA, MorrisR, ParsonsR, TreuschAH, GiovannoniSJ, VerginK. Seasonal dynamics of SAR11 populations in the euphotic and mesopelagic zones of the northwestern Sargasso Sea. ISME J, 2009, 3: 283-295.

[14]

ChurchMJKirchmanDL. Resource control of bacterial dynamics in the sea. Microbial Ecology of the Oceans, 20082New Jersey, HobokenWiley335-382.

[15]

ChurchMJ, ShortCM, JenkinsBD, KarlDM, ZehrJP. Temporal patterns of nitrogenase gene (nifH) expression in the oligotrophic North Pacific Ocean. Appl Environ Microbiol, 2005, 71: 5362-5370.

[16]

ColeJJ, FindlayS, PaceML. Bacterial production in fresh and saltwater ecosystems: a cross-system overview. Mar Ecol Prog Ser, 1988, 43: 1-10.

[17]

CottrellMT, KirchmanDL. Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low-and high-molecular-weight dissolved organic matter. Appl Environ Microbiol, 2000, 66: 1692-1697.

[18]

Dai M, Luo YW, Achterberg EP, Browning TJ, Cai Y, Cao Z, Chai F, Chen B, Church MJ, Ci D, Du C, Gao S, Guo X, Hu Z, Kao S, Laws EA, Lee Z, Lin H, Liu Q, Liu X et al (2023) Upper ocean biogeochemistry of the oligotrophic North PacificSubtropical Gyre: from nutrient sources to carbon export. Rev Geophys 61:e2022RG000800

[19]

Del GiorgioPA, DuarteCM. Respiration in the open ocean. Nat, 2002, 420: 379-384.

[20]

Del GiorgioPA, ColeJJ, CimblerisA. Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems. Nat, 1997, 385: 148-151.

[21]

Delgado-BaquerizoM, ReithF, DennisPG, HamontsK, PowellJR, YoungA, BissettA. Ecological drivers of soil microbial diversity and soil biological networks in the Southern Hemisphere. Ecol, 2018, 99: 583-596.

[22]

DuarteCM, Regaudie-de-GiouxA, ArrietaJM, Delgado-HuertasA, AgustíS. The oligotrophic ocean is heterotrophic. Annu Rev Mar Sci, 2013, 5: 551-569.

[23]

DucklowHKirchmanDL. Bacterial production and biomass in the oceans. Microbial ecology of the oceans, 20004New YorkWiley85-120

[24]

DucklowHW, DoneySC. What is the metabolic state of the oligotrophic ocean? A debate. Annu Rev Mar Sci, 2013, 5: 525-533.

[25]

FaustK, RaesJ. Microbial interactions: from networks to models. Nat Rev Microbiol, 2012, 10: 538-550.

[26]

Fenchel T (2005) Respiration in aquatic protists. In: Del Giorgio PA, Williams P (Eds) Respiration in aquatic ecosystems, 4th edn. OUP, Oxford, pp 47–56

[27]

FengJ, ZengXM, ZhangQZXQ, LiuYR, HuangQ. Soil microbial trait-based strategies drive metabolic efficiency along an altitude gradient. ISME Comm, 2021, 1: 71.

[28]

FuhrmanJA. Microbial community structure and its functional implications. Nat, 2009, 459: 193-199.

[29]

GaoGF, PengD, WuD, ZhangY, ChuH. Increasing inundation frequencies enhance the stochastic process and network complexity of the soil archaeal community in coastal wetlands. Appl Environ Microbiol, 2021, 87: e02560-e2620.

[30]

García-MartínEE, Aranguren-GassisM, KarlDM, Martínez-GarcíaS, RobinsonC, SerretP, TeiraE. Validation of the in vivo iodo-nitro-tetrazolium (INT) salt reduction method as a proxy for plankton respiration. Front Mar Sci, 2019, 6: 220.

[31]

GattusoJP, PeduzziS, PizayMD, TonollaM. Changes in freshwater bacterial community composition during measurements of microbial and community respiration. J Plankton Res, 2002, 24: 1197-1206.

[32]

GilbertJA, SteeleJA, CaporasoJG, SteinbrückL, ReederJ, TempertonB, FieldD. Defining seasonal marine microbial community dynamics. ISME J, 2012, 6: 298-308.

[33]

GiovannoniSJ, TrippHJ, GivanS, PodarM, VerginKL, BaptistaD, MathurEJ. Genome streamlining in a cosmopolitan oceanic bacterium. Sci, 2005, 309: 1242-1245.

[34]

GomesA, GasolJM, EstradaM, Franco-VidalL, Díaz-PérezL, FerreraI, MoránXA. Heterotrophic bacterial responses to the winter–spring phytoplankton bloom in open waters of the NW Mediterranean. Deep-Sea Res Part I, 2015, 96: 59-68.

[35]

GuoC, KeY, ChenB, ZhangS, LiuH. Making comparable measurements of bacterial respiration and production in the subtropical coastal waters. Mar Life Sci Technol, 2022, 4: 414-427.

[36]

HansellDA, CarlsonCA, RepetaDJ, SchlitzerR. Dissolved organic matter in the ocean: a controversy stimulates new insights. Oceanogr, 2009, 22: 202-211.

[37]

HerlemannDP, LabrenzM, JürgensK, BertilssonS, WaniekJJ, AnderssonAF. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J, 2011, 5: 1571-1579.

[38]

HopkinsonCSJr. Shallow-water benthic and pelagic metabolism: evidence of heterotrophy in the nearshore Georgia Bight. Mar Biol, 1985, 87: 19-32.

[39]

HuangY, ChenB, HuangB, ZhouH, YuanY. Potential overestimation of community respiration in the western Pacific boundary ocean: what causes the putative net heterotrophy in oligotrophic systems?. Limnol Oceanogr, 2019, 64: 2202-2219.

[40]

HutchinsDA, FuF. Microorganisms and ocean global change. Nat Microbiol, 2017, 2: 1-11.

[41]

ImaiK, NojiriY, TsurushimaN, SainoT. Time series of seasonal variation of primary productivity at station KNOT (44°N, 155°E) in the sub-arctic western North Pacific. Deep-Sea Res Part II, 2002, 49: 5395-5408.

[42]

KarlDM, ChurchMJ. Microbial oceanography and the Hawaii Ocean Time-series programme. Nat Rev Microbiol, 2014, 12: 699-713.

[43]

KarlDM, BjörkmanKM, DoreJE, FujiekiL, HebelDV, HoulihanT, TupasLM. Ecological nitrogen-to-phosphorus stoichiometry at station ALOHA. Deep-Sea Res Part II, 2001, 48: 1529-1566.

[44]

KarlDM, BeversdorfL, BjörkmanKM, ChurchMJ, MartinezA, DelongEF. Aerobic production of methane in the sea. Nat Geosci, 2008, 1: 473-478.

[45]

KimB, KimSH, KwakJH, KangCK, LeeSH, HyunJH. Heterotrophic bacterial production, respiration, and growth efficiency associated with upwelling intensity in the Ulleung Basin, East Sea. Deep-Sea Res Part II, 2017, 143: 24-35.

[46]

KirchmanDL, KeelRG, SimonM, WelschmeyerNA. Biomass and production of heterotrophic bacterioplankton in the oceanic subarctic Pacific. Deep-Sea Res Part I, 1993, 40: 967-988.

[47]

Kletou D, Hall-Spencer JM (2012) Threats to ultraoligotrophic marine ecosystems. In A Cruzado (Ed) Marine Ecosystems, 1st edn. InTech, Rijeka, Croatia, pp 1–34

[48]

KorlevićM, ŠuprahaL, LjubešićZ, HenderiksJ, CiglenečkiI, DautovićJ, OrlićS. Bacterial diversity across a highly stratified ecosystem: a salt-wedge Mediterranean estuary. Syst Appl Microbiol, 2016, 39: 398-408.

[49]

LadauJ, SharptonTJ, FinucaneMM, JospinG, KembelSW, O’dwyerJ, PollardKS. Global marine bacterial diversity peaks at high latitudes in winter. ISME J, 2013, 7: 1669-1677.

[50]

LangfelderP, HorvathS. Fast R functions for robust correlations and hierarchical clustering. J Stat Soft, 2012, 46. i11

[51]

LetelierRM, DoreJE, WinnCD, KarlDM. Seasonal and interannual variations in photosynthetic carbon assimilation at Station. Deep-Sea Res Part II, 1996, 43: 467-490.

[52]

LiuH, ImaiK, SuzukiK, NojiriY, TsurushimaN, SainoT. Seasonal variability of picophytoplankton and bacteria in the western subarctic Pacific Ocean at station KNOT. Deep-Sea Res Part II, 2002, 49: 5409-5420.

[53]

LoucaS, PolzMF, MazelF, AlbrightMB, HuberJA, O’ConnorMI, ParfreyLW. Function and functional redundancy in microbial systems. Nat Ecol Evol, 2018, 2: 936-943.

[54]

LurgiM, ThomasT, WemheuerB, WebsterNS, MontoyaJM. Modularity and predicted functions of the global sponge-microbiome network. Nat Comm, 2019, 10: 992.

[55]

MarieD, PartenskyF, JacquetS, VaulotD. 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: 186-193.

[56]

Martínez-GarcíaS, FernándezE, Aranguren-GassisM, TeiraE. In vivo electron transport system activity: a method to estimate respiration in natural marine microbial planktonic communities. Limnol Oceanogr Methods, 2009, 7: 459-469.

[57]

MassanaR, PedrόsttAliόC, CasamayorEO, GasolJM. Changes in marine bacterioplankton phylogenetic composition during incubations designed to measure biogeochemically significant parameters. Limnol Oceanogr, 2001, 46: 1181-1188.

[58]

Munson-McGeeJH, LindsayMR, SintesE, BrownJM, D’AngeloT, BrownJ, StepanauskasR. Decoupling of respiration rates and abundance in marine prokaryoplankton. Nat, 2022, 612: 764-770.

[59]

Odate T, Furuya K (1995) Primary production and community respiration in the subarctic water of the western North Pacific. In: Sakai H, Nozaki Y (Eds) Biogeochemical Processes and Ocean Flux in the Western Pacific, 4th edn. TERRAPUB, Tokyo, pp: 239–253

[60]

PolovinaJJ, HowellEA, AbecassisM. Ocean’s least productive waters are expanding. Geophys Res Lett, 2008, 35: L03618.

[61]

PolymenakouPN, BertilssonS, TselepidesA, StephanouEG. Links between geographic location, environmental factors, and microbial community composition in sediments of the Eastern Mediterranean Sea. Microb Ecol, 2005, 49: 367-378.

[62]

PomeroyLR, SheldonJE, SheldonWMJr. Changes in bacterial numbers and leucine assimilation during estimations of microbial respiratory rates in seawater by the precision Winkler method. Appl Environ Microbio, 1994, 60: 328-332.

[63]

QiuL, ZhangQ, ZhuH, ReichPB, BanerjeeS, van der HeijdenMG, WeiX. Erosion reduces soil microbial diversity, network complexity and multifunctionality. ISME J, 2021, 15: 2474-2489.

[64]

RamAP, NairS, ChandramohanD. Bacterial growth efficiency in the tropical estuarine and coastal waters of Goa, southwest coast of India. Microb Ecol, 2003, 45: 88-96.

[65]

RivkinRB, LegendreL. Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Sci, 2001, 291: 2398-2400.

[66]

RobinsonCKirchmanDL. Heterotrophic bacterial respiration. Microbial Ecology of the Oceans, 20082New Jersey, HobokenWiley299-334.

[67]

RobinsonC, SteinbergDK, AndersonTR, ArísteguiJ, CarlsonCA, FrostJR, ZhangJ. Mesopelagic zone ecology and biogeochemistry-a synthesis. Deep-Sea Res Part II, 2010, 57: 1504-1518.

[68]

RoccaJD, HallEK, LennonJT, EvansSE, WaldropMP, CotnerJB, WallensteinMD. Relationships between protein-encoding gene abundance and corresponding process are commonly assumed yet rarely observed. ISME J, 2015, 9: 1693-1699.

[69]

SarmentoH, GasolJM. Use of phytoplankton-derived dissolved organic carbon by different types of bacterioplankton. Environ Microbiol, 2012, 14: 2348-2360.

[70]

SchapiraM, PolletT, MitchellJG, SeurontL. Respiration rates in marine heterotrophic bacteria relate to the cytometric characteristics of bacterioplankton communities. J Mar Biol Assoc UK, 2009, 89: 1161-1169.

[71]

ServaisP, AgoguéH, CourtiesC, JouxF, LebaronP. Are the actively respiring cells (CTC+) those responsible for bacterial production in aquatic environments?. FEMS Microbiol Ecol, 2001, 35: 171-179.

[72]

SteeleJA, CountwayPD, XiaL, VigilPD, BemanJM, KimDY, FuhrmanJA. Marine bacterial, archaeal and protistan association networks reveal ecological linkages. ISME J, 2011, 5: 1414-1425.

[73]

TeiraE, Martínez-GarcíaS, CarreiraC, MoránXA. Changes in bacterioplankton and phytoplankton community composition in response to nutrient additions in coastal waters off the NW Iberian Peninsula. Mar Ecol Prog Ser, 2011, 426: 87-104.

[74]

ThingstadTF, LignellR. Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat Microb Ecol, 1997, 13: 19-27.

[75]

WelschmeyerNA. Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr, 1994, 39: 1985-1992.

[76]

WilliamsPJ, QuayPD, WestberryTK, BehrenfeldMJ. The oligotrophic ocean is autotrophic. Annu Rev Mar Sci, 2013, 5: 535-549.

[77]

WuW, LogaresR, HuangB, HsiehCH. Abundant and rare picoeukaryotic sub-communities present contrasting patterns in the epipelagic waters of marginal seas in the northwestern Pacific Ocean. Environ Microbiol, 2017, 19: 287-300.

[78]

WuMH, ChenSY, ChenJW, XueK, ChenSL, WangXM, WangYF. Reduced microbial stability in the active layer is associated with carbon loss under alpine permafrost degradation. PNAS, 2021, 118. e2025321118

[79]

XiaX, GuoW, LiuH. Dynamics of the bacterial and archaeal communities in the Northern South China Sea revealed by 454 pyrosequencing of the 16S rRNA gene. Deep-Sea Res Part II, 2015, 117: 97-107.

[80]

XuJ, LiX, ShiZ, LiR, LiQ. Bacterial carbon cycling in the river plume in the northern South China Sea during summer. J Geophys Res Oceans, 2018, 123: 8106-8121.

[81]

XuC, XiangM, ChenB, HuangY, QiuG, ZhangY, WangH, HuangB. Constraining the twilight zone remineralization in the South China Sea basin: Insights from the multi-method intercomparison. Prog Oceanogr, 2024, 228. 103316

[82]

YamadaK, IshizakaJ, YooS, KimHC, ChibaS. Seasonal and interannual variability of sea surface Chl a concentration in the Japan/East Sea (JES). Prog Oceanogr, 2004, 61: 193-211.

[83]

YilmazP, ParfreyLW, YarzaP, GerkenJ, PruesseE, QuastC, GlöcknerFO. The SILVA and “all-species living tree project (LTP)” taxonomic frameworks. Nucleic Acids Res, 2014, 42: D643-D648.

[84]

ZhangL, Delgado-BaquerizoM, ShiY, LiuX, YangY, ChuH. Co-existing water and sediment bacteria are driven by contrasting environmental factors across glacier-fed aquatic systems. Water Res, 2021, 198. 117139

RIGHTS & PERMISSIONS

The Author(s)

AI Summary AI Mindmap
PDF

164

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/