To clarify horizontal variability and regulation of bacterial production (BP), we investigated BP and environmental variables along three east–west transects (lines 12, 15, and 17) covering inshore/offshore stations in Lake Biwa, Japan, during four seasons using 15N-labeled deoxyadenosine for measuring BP. In winter, surface BP along Line 12 (southern transect) was higher than Lines 15 and 17 (central and northern transects) and reflected the water-temperature distribution. Additionally, any nutrients and dissolved organic carbon did not correlate to BP, suggesting water temperature primarily regulated BP in winter. In spring, surface BP was higher at eastern inshore stations, near large agricultural fields, and was correlated with nutrient concentrations rather than water temperature, suggesting that the limitation shifted to nutrient availability. In summer, surface BP at offshore stations along Lines 15 and 17 was notably lower than the other stations, and the horizontal heterogeneity became largest (maximum to minimum BP ratio = 9.5, compared to 2.8 ~ 4.1 in the other seasons). The BP was also positively correlated to nutrient concentrations, especially phosphorus. Surface BP in autumn also showed higher values at eastern stations as well as spring and positively correlated to phosphorus concentration. Additionally, there was a negative relationship between BP and water temperature, suggesting that bacterial growth was enhanced by groundwater seepage at the eastern stations. The results suggest that the horizontal distribution is characterized by a north–south distribution with a temperature gradient in winter, and allochthonous nutrient loading determines horizontal BP variations in the other seasons in this lake.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Price excludes VAT (USA)
Tax calculation will be finalised during checkout.
Attermeyer K, Grossart H, Flury S, Premke K (2017) Bacterial processes and biogeochemical changes in the water body of kettle holes—mainly driven by autochthonous organic matter? Auqat Sci 79:675–687. https://doi.org/10.1007/s00027-017-0528-1
Azam F (1998) Microbial control of oceanic carbon flux: the plot thickens. Science 280:694–696. https://doi.org/10.1126/science.280.5364.694
Benner R, Biddanda B (1998) Photochemical transformations of surface and deep marine dissolved organic matter: effects on bacterial growth. Limnol Oceanogr 43:1373–1378. https://doi.org/10.4319/lo.1922.214.171.1243
Bischof SM et al (2019) Further development of a specific conductivity approach to measure groundwater discharge area within lakes. J Am Water Wrokds Ass 55:485–496. https://doi.org/10.1111/1752-1688.12730
Blees J, Niemann H, Wenk CB, Zopfi J, Schubert CJ, Jenzer JS, Veronesi M, Lehmann MF (2014) Bacterial methanotrophs drive the formation of a seasonal anoxic benthic nepheloid layer in an alpine lake. Limnol Oceanogr 59:1410–1420. https://doi.org/10.4319/lo.2014.59.4.1410
Endoh S, Okumura Y (1993) Gyre system in Lake Biwa derived from recent current measurements. Jpn J Limnol 54:191–197. https://doi.org/10.3739/rikusui.54.191
Endoh S, Imawaki S, Kunishi H (1979) Studies on the internal waves by observing the time variations of water temperature in Lake Biwa. Disaster Prev Res Inst Annu 22:601–609 (in Japanese)
Endoh S et al (1995) Wind fields over Lake Biwa and their effect on water circulation. Jpn J Limnol 56:269–278. https://doi.org/10.3739/rikusui.56.269
Filippini M, Buesing N, Gessner MO (2008) Temporal dynamics of freshwater bacterio- and virioplankton along a littoral-pelagic gradient. Freshw Biol 53:1114–1125. https://doi.org/10.1111/j.1365-2427.2007.01886.x
Fouilland E, Mostajir B (2010) Revisited phytoplanktonic carbon dependency of heterotrophic bacteria in freshwaters, transitional, coastal and oceanic waters. FEMS Microbiol Ecol 73:419–429. https://doi.org/10.1111/j.1574-6941.2010.00896.x
Güde H (1990) Bacterial production and the flow of organic matter in lake constance. In: Tilzer MM, Serruya C (eds) Large lakes: ecological structure and function. Springer, Berlin Heidelberg, Berlin
Goosen NK, van Rijswijk P, Kromkamp J, Peene J (1997) Regulation of annual variation in heterotrophic bacterial production in the Schelde estuary (SW Netherlands). Aquat Microb Ecol 12:223–232. https://doi.org/10.3354/ame012223
Gurung TB, Urabe J (1999) Temporal and vertical difference in factors limiting growth rate of heterotrophic bacteria in Lake Biwa. Microb Ecol 38:136–145. https://doi.org/10.1007/s002489900167
Gurung TB, Urabe J, Nozaki K, Yoshimizu C, Nakanishi M (2002) Bacterioplankton production in a water column of Lake Biwa. Lakes Reserv 7:317–323. https://doi.org/10.1046/j.1440-1770.2002.00197.x
Hayakawa K (2004) Seasonal variations and dynamics of dissolved carbohydrates in Lake Biwa. Org Geochem 35:169–179. https://doi.org/10.1016/j.orggeochem.2003.09.002
Kawasaki N et al (2011) Fast and precise method for HPLC-size exclusion chromatography with UV and TOC (NDIR) detection: importance of multiple detectors to evaluate the characteristics of dissolved organic matter. Water Res 45:6240–6248. https://doi.org/10.1016/j.watres.2011.09.021
Kim C, Nishimura Y, Nagata T (2007) High potential activity of alkaline phosphatase in the benthic nepheloid layer of a large mesotrophic lake: implications for phosphorus regeneration in oxygenated hypolimnion. Aquat Microb Ecol 49:303–311. https://doi.org/10.3354/ame01137
Kumagai M, Tsuda R, Fukagae K (1995) Dynamics of the turbid benthic boundary layer. In: Okuda S, Imberger J, Kumagai M (eds) Physical processes in a large lake: Lake Biwa, Japan. American Geophysical Union, Washington, DC, pp 87–99
Mostofa KM, Yoshioka T, Konohira E, Tanoue E (2007) Dynamics and characteristics of fluorescent dissolved organic matter in the groundwater, river and lake water. Water Air Soil Pollut 184:157–176. https://doi.org/10.1007/s11270-007-9405-1
Murakami Y, Otsuka S, Senoo K (2009) Abundance and community structure of sphingomonads in leaf residues and nearby bulk soil. Microbes Environ. https://doi.org/10.1264/jsme2.ME10114 (advpub:1006160198-1006160198)
Nagata T (1986) Carbon and nitrogen content of natural planktonic bacteria. Appl Environ Microbiol 52:28–32. https://doi.org/10.1128/aem.52.1.28-32.1986
Nagata T (1987) Production rate of planktonic bacteria in the north basin of lake biwa, Japan. Appl Environ Microbiol 53:2872–2882. https://doi.org/10.1128/AEM.53.12.2872-2882.1987
Nojiri Y (1987) Progress in water quality analysis (3). J Groundwater Hydrol 29:107–111. https://doi.org/10.5917/jagh1987.29.107
Otsuki A, Goma R, Aizaki M, Nojiri Y (1993) Seasonal and spatial variations of dissolved nitrogenous nutrient concentrations in hypertrophic shallow lake, with special reference to dissolved organic nitrogen. Internationale Vereinigung Für Theoretische Und Angewandte Limnologie: Verhandlungen 25:187–192. https://doi.org/10.1080/03680770.1992.11900089
Pomeroy LR, Wiebe WJ (2001) Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria. Aquat Microb Ecol 23:187–204. https://doi.org/10.3354/ame023187
Ram ASP, Nishimura Y, Tomaru Y, Nagasaki K, Nagata T (2010) Seasonal variation in viral-induced mortality of bacterioplankton in the water column of a large mesotrophic lake (Lake Biwa, Japan). Aquat Microb Ecol 58:249–259. https://doi.org/10.3354/ame01381
Reichart I, Simon M (1996) Horizontal variability of bacterioplankton growth dynamics in a large lake. Aquat Microb Ecol 11:31–41. https://doi.org/10.3354/ame011031
Reitner B, Herzig A, Herndl GJ (1999) Dynamics in bacterioplankton production in a shallow, temperate lake (Lake Neusiedl, Austria): evidence for dependence on macrophyte production rather than on phytoplankton. Aquat Microb Ecol 19:245–254. https://doi.org/10.3354/ame019245
Ritzrau W (1996) Microbial activity in the benthic boundary layer: Small-scale distribution and its relationship to the hydrodynamic regime. J Sea Res 36:171–180. https://doi.org/10.1016/S1385-1101(96)90787-X
Sato Y, Okamoto T, Hayakawa K, Okubo T, Komatsu E (2016) The source of refractory organic matters in Lake Biwa: estimation by biodegradation assay in generation sources and box model. J Jap Soc Water Environ 39:17–28. https://doi.org/10.2965/jswe.39.17 (in Japanese)
Scavia D, Laird GA (1987) Bacterioplankton in Lake Michigan: dynamics, controls, and significance to carbon flux. Limnol Oceanogr 32:1017–1033. https://doi.org/10.4319/lo.19126.96.36.1997
Shiah FK, Ducklow HW (1994a) Temperature and substrate regulation of bacterial abundance, production and specific growth-rate in Chesapeake Bay, USA. Mar Ecol Prog Ser 103:297–308. https://doi.org/10.3354/meps104297
Shiah FK, Ducklow HW (1994b) Temperature regulation of heterotrophic bacterioplankton abundance, production, and specific growth rate in Chesapeake Bay. Limnol Oceanogr 39:1243–1258. https://doi.org/10.4319/lo.19188.8.131.523
Shiga-Prefecture (2017) Environmental white paper in 2017 (reference). pp 11–78. https://www.pref.shiga.lg.jp/file/attachment/4016451.pdf. Accessed 1 Feb 2019 (in Japanese)
Shimotori K et al (2016) Quantification and characterization of coastal dissolved organic matter by high-performance size exclusion chromatography with ultraviolet absorption, fluorescence, and total organic carbon analyses. Limnol Oceanogr-Meth 14:637–648. https://doi.org/10.1002/lom3.10118
Tanentzap AJ et al (2017) Terrestrial support of lake food webs: synthesis reveals controls over cross-ecosystem resource use. Sci Adv 3:e1601765. https://doi.org/10.1126/sciadv.1601765
Taniguchi M, Tase N (1999) Nutrient discharge by groundwater and rivers into Lake Biwa, Japan. IAHS Publ 257:67–74
They NH, Marques DdM (2019) The structuring role of macrophytes on plankton community composition and bacterial metabolism in a large subtropical shallow lake. Acta Limnol Bras. https://doi.org/10.1590/s2179-975x10017
Tsuchiya K (2020) Development and application of methods for measuring bacterial production as an alternative to radioisotopes. Chikyu Kankyo 25:43–52 (in Japanese)
Tsuchiya K et al (2015) New radioisotope-free method for measuring bacterial production using [15N5]-2′-deoxyadenosine and liquid chromatography mass spectrometry (LC–MS) in aquatic environments. J Oceanogr 71:675–683. https://doi.org/10.1007/s10872-015-0310-8
Tsuchiya K et al (2019) Seasonal variability and regulation of bacterial production in a shallow eutrophic lake. Limnol Oceanogr 64:2441–2454. https://doi.org/10.1002/lno.11196
Tsuchiya K et al (2020a) Incorporation characteristics of exogenous 15N-labeled thymidine, deoxyadenosine, deoxyguanosine and deoxycytidine into bacterial DNA. PLoS ONE 15:e0229740. https://doi.org/10.1371/journal.pone.0229740
Tsuchiya K et al (2020b) Decrease in bacterial production over the past three decades in the north basin of Lake Biwa, Japan. Limnology 21:87–96. https://doi.org/10.1007/s10201-019-00582-2
Tsuda R (1995) Turbidity in the North and South Basins. In: Okuda S, Imberger J, Kumagai M (eds) Physical processes in a large lake: Lake Biwa, Japan. American Geophysical Union, Washington, DC, pp 77–86
Wold S, Sjöström M, Eriksson L (2001) PLS-regression: a basic tool of chemometrics. Chemom Intell Lab Syst 58:109–130. https://doi.org/10.1016/S0169-7439(01)00155-1
Wylie JL, Currie DJ (1991) The relative importance of bacteria and algae as food sources for crustacean zooplankton. Limnol Oceanogr 36:708–728. https://doi.org/10.4319/lo.1991.36.4.0708
This research was supported by the Environment Research and Technology Development Fund (grant number 5-1607) of the Ministry of the Environment, Japan. This work was also partly supported by JSPS KAKENHI grant numbers JP15K21449, JP17K12814, JP17J11577, and JP20K12140. The authors declare that there is no conflict of interest.
Handling Editor: Takafumi Kataoka.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Tsuchiya, K., Tomioka, N., Komatsu, K. et al. Horizontal variability and regulation of bacterial production in Lake Biwa, Japan. Limnology 23, 231–243 (2022). https://doi.org/10.1007/s10201-021-00687-7
- Phosphorus limitation
- External loading
- Seasonal limitation shift