Abstract
In Lake Biwa, the largest lake in Japan, external pollutant loads have decreased since the 1980s, leading to improved water quality, such as reduction in biochemical oxygen demand (BOD) and PO43− concentrations. We examined long-term variation of bacterial production (BP) under these environmental changes from 2016–2017 in the north basin of Lake Biwa. BP was estimated by measuring the incorporation of stable isotope 15N-labeled deoxyadenosine (15N-dA) from June 2016 and December 2017 and compared with measurements from 1986 and 1997–1998. In 1986, BP was measured by following 3H-labeled thymidine (3H-TdR) incorporation and in 1997–1998 by tracking bacterial abundance in incubations and calculating specific growth rates (μ). To allow direct comparison of 15N-dA and 3H-TdR incorporation rates, we determined a conversion factor. To estimate μ in 2016–2017, we determined a factor for converting 15N-dA incorporation to cell number increase. In 2016–2017, the 15N-dA incorporation rate ranged from 0.13 to 30.7 pmol l−1 h−1 and μ ranged from 0.016 to 0.70 day−1. BP values from 3H-TdR incorporation rates in 1986 and μ in 1997–1998 were 4.6 and 2.1 times BP values in 2016–2017, respectively, confirming the decrease in BP over the past 3 decades in Lake Biwa. Water quality data showed only low decrease rates for BOD and total phosphorus concentration from the 1980s, whereas the rate of decrease for PO43− concentrations was equivalent to that of BP. BP and decomposition of organic matter are known to be strongly P-limited in Lake Biwa. Our results suggest that the decrease in BP can be explained by a reduction in readily bioavailable PO43−. Organic phosphorus can also be an important P-source for BP under conditions with very low PO43− concentrations (nM), and changes in the bioavailability of organic phosphorus might have also regulated BP dynamics.
Similar content being viewed by others
References
Azam F (1998) Microbial control of oceanic carbon flux: the plot thickens. Science 280:694–696
Badawy MI, Ali M (2006) Fenton's peroxidation and coagulation processes for the treatment of combined industrial and domestic wastewater. J Hazard Mater 136:961–966
Björkman KM, Karl DM (2003) Bioavailability of dissolved organic phosphorus in the euphotic zone at Station ALOHA, North Pacific Subtropical Gyre. Limnol Oceanogr 48:1049–1057
Brittain AM, Karl DM (1990) Catabolism of tritiated-thymidine by aquatic microbial communities and incorporation of tritium into RNA and protein. Appl Environ Microbiol 56:1245–1254
Carlsson P, Caron DA (2001) Seasonal variation of phosphorus limitation of bacterial growth in a small lake. Limnol Oceanogr 46:108–120
Farjalla VF, Esteves FA, Bozelli RL, Roland F (2002) Nutrient limitation of bacterial production in clear water Amazonian ecosystems. Hydrobiologia 489:197–205
Fuhrman JA, Azam F (1982) Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters—evaluation and field results. Mar Biol 66:109–120
Furuta S, Ikegaya H, Ikeda S, Fujiwara N, Okamoto T, Ichise S, Bamba D, Kishimoto N, Imai A (2014) Analysis of biodegradation characteristics of Staurastrum arctiscon (Desmidiaceae) in Lake Biwa. J Jpn Soc Water Environ 37:103–109
Granéli W, Bertilsson S, Philibert A (2004) Phosphorus limitation of bacterial growth in high Arctic lakes and ponds. Aquat Sci 66:430–439
Güde H (1988) Direct and indirect influences of crustacean zooplankton on bacterioplankton of Lake Constance. Hydrobiologia 159:63–73
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
Gurung TB, Nakanishi M, Urabe J (2000) Seasonal and vertical difference in negative and positive effects of grazers on heterotrophic bacteria in Lake Biwa. Limnol Oceanogr 45:1689–1696
Gurung TB, Kagami M, Yoshida T, Urabe J (2001) Relative importance of biotic and abiotic factors affecting bacterial abundance in Lake Biwa: an empirical analysis. Limnology 2(1):19–28
Hayakawa K (2004) Seasonal variations and dynamics of dissolved carbohydrates in Lake Biwa. Org Geochem 35:169–179
Hoch B, Berger B, Kavka G, Herndl GJ (1995) Remineralization of organic matter and degradation of the organic fraction of suspended solids in the River Danube. Aquat Microb Ecol 09:279–288
Hsieh CH, Ishikawa K, Sakai Y, Ishikawa T, Ichise S, Yamamoto Y, Kuo TC, Park HD, Yamamura N, Kumagai M (2010) Phytoplankton community reorganization driven by eutrophication and warming in Lake Biwa. Aquat Sci 72:467–483
Ichise S, Ikegaya H, Furuta S, Fujiwara N, Ikeda S, Kishimoto N, Nishimura O (2013) Analysis of long-term variation of phytoplankton biovolume and gelatinous sheath volume in Lake Biwa. J Jpn Biol Soc Water Waste 49:65–74
Jonas RB (1997) Bacteria, dissolved organics and oxygen consumption in salinity stratified Chesapeake Bay, an anoxia paradigm. Am Zool 37:612–620
Jonas RB, Tuttle JH (1990) Bacterioplankton and organic carbon dynamics in the lower mesohaline Chesapeake Bay. Appl Environ Microbiol 56:747–757
Kirchman DL (1992) Incorporation of thymidine and leucine in the subarctic Pacific: application to estimating bacterial production. Mar Ecol Prog Ser 82:301–309
Kirchman D, Knees E, Hodson R (1985) Leucine incorporation and its potential as a measure of protein-synthesis by bacteria in natural aquatic systems. Appl Environ Microbiol 49:599–607
Kishimoto N, Ueno K (2011) Influence of phosphorus concentration on the biodegradation of dissolved organic matter in Lake Biwa, Japan. J Water Environ Technol 9:215–223
Kishimoto N, Ichise S, Suzuki K, Yamamoto C (2013) Analysis of long-term variation in phytoplankton biovolume in the northern basin of Lake Biwa. Limnology 14:117–128
Legendre P (2001) Model II regression—user’s guide. Département de sciences biologiques, Université de Montréal
Markosova R, Benediktova M, Volkova A (1990) Time- and vertical distribution of bacterioplankton in a shallow eutrophic reservoir. Water Res 24:1057–1067
Nagata T (1987) Production rate of planktonic bacteria in the north basin of lake biwa, Japan. Appl Environ Microbiol 53:2872–2882
Nohara K, Baba T, Murai H, Kobayashi Y, Suzuki T, Tateishi Y, Matsumoto M, Nishimura N, Sano T (2011) Global DNA methylation in the mouse liver is affected by methyl deficiency and arsenic in a sex-dependent manner. Arch Toxicol 85:653–661
Pradeep Ram AS, 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
Robarts RD, Waiser MJ, Hadas O, Zohary T, Maclntyre S (1998) Relaxation of phosphorus limitation due to typhoon-induced mixing in two morphologically distinct basins of Lake Biwa, Japan. Limnol Oceanogr 43:1023–1036
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 Jpn Soc Water Environ 39:17–28
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
Shiga-Prefecture, Kyoto-Prefecture (2017) Seventh term protection plan of water quality of Lake Biwa. pp 1–36. https://www.env.go.jp/water/Biwa-7.pdf. Accessed 1 June 2018
Smith DC, Azam F (1992) A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar Microb Food Webs 6:107–114
Smith EM, Prairie YT (2004) Bacterial metabolism and growth efficiency in lakes: the importance of phosphorus availability. Limnol Oceanogr 49:137–147
Tezuka Y (1992) Recent trend in the eutrophication of the north basin of Lake Biwa. Jpn J Limnol 53:139–144
Tinta T, Christiansen LS, Konrad A, Liberles DA, Turk V, Munch-Petersen B, Piskur J, Clausen AR (2012) Deoxyribonucleoside kinases in two aquatic bacteria with high specificity for thymidine and deoxyadenosine. FEMS Microbiol Lett 331:120–127
Toolan T, Wehr JD, Findlay S (1991) Inorganic phosphorus stimulation of bacterioplankton production in a meso-eutrophic lake. Appl Environ Microbiol 57:2074–2078
Tsuchiya K, Sano T, Kawasaki N, Fukuda H, Tomioka N, Hamasaki K, Tada Y, Shimode S, Toda T, Imai A (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
Tsuchiya K, Sano T, Tomioka N, Kohzu A, Komatsu K, Shinohara R, Takamura N, Nakagawa M, Sugai Y, Kuwahara VS, Toda T, Fukuda H, Imai A (2019) Seasonal variability and regulation of bacterial production in a shallow eutrophic lake. Limnol Oceanogr 9999:1–14. https://doi.org/10.1002/lno.11196
Urabe J, Yoshida T, Gurung TB, Sekino T, Tsugeki N, Nozaki K, Maruo M, Nakayama E, Nakanishi M (2005) The production-to-respiration ratio and its implication in Lake Biwa, Japan. Ecol Res 20:367–375
Vollertsen J, Hvitved-Jacobsen T (2002) Biodegradability of wastewater—a method for COD-fractionation. Water Sci Technol 45:25
Wylie JL, Currie DJ (1991) The relative importance of bacteria and algae as food sources for crustacean zooplankton. Limnol Oceanogr 36:708–728
Yamada E, Ohara S, Uehara T, Hirota T, Hatori N, Fuse Y, Aoki S (2012) Biodegradation of dissolved organic matter (DOM) released from phytoplankton in Lake Biwa. Anal Sci 28:675–681
Yoshida T, Gurung T, Kagami M, Urabe J (2001) Contrasting effects of a cladoceran (Daphnia galeata) and a calanoid copepod (Eodiaptomus japonicus) on algal and microbial plankton in a Japanese lake, Lake Biwa. Oecologia 129:602–610
Acknowledgements
This research was supported by the Environment Research and Technology Development Fund (Grant No. 5-1607) of the Ministry of the Environment, Japan. This work was also partly supported by Grants-in-Aid for Scientific Research (JP15K21449, JP17K12814, and JP17J11577) of the Japan Society for the Promotion of Science.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Kunihiro Okano.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Tsuchiya, K., Tomioka, N., Sano, T. et al. Decrease in bacterial production over the past three decades in the north basin of Lake Biwa, Japan. Limnology 21, 87–96 (2020). https://doi.org/10.1007/s10201-019-00582-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10201-019-00582-2