Sedimentary Microbial Community Dynamics in a Regulated Stream - East Fork of the Little Miami River, Ohio

Environmental Microbiology (2003) 5 (4), 256–266 © 2003 Society for Applied Microbiology and Blackwell Publishing Ltd Blackwell Science, LtdOxford, UKEMIEnvironmental Microbiology 1462-2912Blackwell Publishing Ltd, 20035Original Article Microbial community dynamics in stream sedimentsS. D. Sutton and R. H. Findlay Received 13 June, 2002; revised 4 October, 2002; accepted 18 October, 2002. *For correspondence. E-mail; Tel. ( + 1) 513 529 5422;
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  Environmental Microbiology (2003) 5 (4), 256–266 © 2003 Society for Applied Microbiology and Blackwell Publishing Ltd Blackwell Science, LtdOxford, UKEMIEnvironmental Microbiology 1462-2912Blackwell Publishing Ltd, 20035Original Article Microbial community dynamics in stream sedimentsS.D.Sutton and R.H.Findlay Received 13 June, 2002; revised 4 October, 2002; accepted 18October, 2002. *For correspondence. E-mail;Tel. ( + 1) 513 529 5422; Fax ( + 1) 513 529 2431. † Present address:Eli Lilly and Company, Lilly Research Laboratories DC6065,Indianapolis, IN 46285, USA. Sedimentary microbial community dynamics ina regulated stream: East Fork of the LittleMiami River, Ohio Susan D. Sutton †  and Robert H. Findlay* Department of Microbiology, Miami University, Oxford, Ohio 45056, USA. SummaryA field study was conducted in the Lower East Fork of the Little Miami River, a regulated stream inClermont county, Ohio, to determine how changesin streamflow, water temperature and photo-periodaffect sediment microbial community structure. Sur-face sediment cores were collected from samplingstations spanning 60 river kilometers three to fourtimes per year between October 1996 and October1999. During the final year of the field study, watertemperature, water depth, conductivity, total sus-pended solids, dissolved organic carbon, instanta-neous streamflow velocity, sediment grain size andsediment organic matter were determined. Totalmicrobial biomass was measured using the phospho-lipid phosphate technique (PLP) and ranged between2 and 134 nmol PLP ã g ---- 1  dry weight sediment with amean of 25 nmol PLP ã g ---- 1 . Microbial communitystructure was determined using the phospholipidfatty acid analysis and indicated seasonal shifts insedimentary microbial community composition.January to June sedimentary microbial biomasswas predominately prokaryotic (60% ±±±±  2), whereasmicroeukaryotes dominated samples collected duringthe late summer (55% ±±±±  2.4) and fall (60% ±±±±  2). Thesechanges were correlated with stream discharge andwater temperature. Microbial community structurevaried spatially about a reservoir with prokaryotic bio-mass dominant at upstream stations and eukaryoticbiomass dominant at downstream stations. Thesefindings reveal that sedimentary microbial communi-ties in streams are dynamic responding to the sea-sonal variation of environmental factors.Introduction Environmental factors such as climate, season, watershedhydrology, geomorphology and land use are importanteffectors of stream processes. Other abiotic factors suchas streamflow velocity and water temperature can varydramatically throughout the year and influence the sea-sonal dynamics of both biotic and abiotic parameters.Historically, investigators have focused on how these envi-ronmental factors impact on fish, macroinvertebrates andphototrophic communities in streams, and attempted touse these organisms as bioindicators of stream health(Ford, 1989; Biggs, 1996; 2000; Dyer et al  ., 1998).Dissolved organic material is a primary biologic sub-strate for stream metabolism (Kaplan and Newbold,1993). Heterotrophic bacteria consume this resourcedirectly and they are therefore important mediators ofstream energy flow. Recently, researchers have begun toinvestigate determinants of prokaryotic community com-position and physiologic status in streams and rivers(Guckert et al  ., 1992; Lemke and Leff, 1999; Brümmer et al  ., 2000) but most studies have focused on the effectsof pollution at small spatial and temporal scales. Informa-tion on the long-term seasonal dynamics of microbialcommunities that describes both prokaryote and microeu-karyote components is lacking and, consequently, themicrobial ecology of lotic systems is poorly understood(Leff, 1994).Our objectives were to determine natural patterns ofseasonal variation in sedimentary microbial biomass andcommunity structure and evaluate the potential impact ofregulated flow in a mid-order stream in south-west Ohio.During a three-year field study (October 1996–October1999), we used phospholipid phosphate (PLP) and phos-pholipid fatty acid (PLFA) analysis to quantify sedimentarymicrobial biomass and identify patterns of variation incommunity structure at six stations along a 60 km sectionof the East Fork Little Miami River. This river has beendesignated an exceptional warm-water habitat by the OhioEnvironmental Protection Agency; it is well oxygenatedand contains moderate levels (for Ohio) of dissolved nutri-ents (Table 1). Three of the six stations were at distantlocations (greater than 5 km) downstream of an artificialreservoir (Harsha Lake) where mainstem streamflow was  Microbial community dynamics in stream sediments  257  © 2003 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology  , 5 , 256–266 regulated. In addition to seasonal dynamics, we deter-mined the relative contribution of prokaryotes andmicroeukaryotes to total viable biomass. During the latersampling dates (September 1998 until October 1999) wemeasured water temperature, water depth, conductivity,instantaneous streamflow velocity, total suspended solids,dissolved organic carbon, sediment particle size and sed-iment organic matter. Historical stream discharge datawere obtained from the U.S. Geological Survey. Theseenvironmental parameters were investigated as proximaldeterminants of the observed changes in sedimentarymicrobial biomass and community composition. Results Determinants of microbial distribution and abundance  The above environmental parameters (eight measuredparameters plus mean 7-day discharge) were evaluatedfor seasonal trends. Water temperature, conductivity, totalsuspended solids and mean 7-day discharge showed sig-nificant changes with sampling date. We grouped sam-pling dates, a posteriori  , into four seasonal groups basedon unique combinations of water temperature and mean7-day discharge (Table 2). Subsequently, mean 7-day dis-charge is referred to as streamflow and the a posteriori  groupings are referred to as seasonal sampling intervals.Data for each measured environmental determinantwere grouped according to season and position (upstreamor downstream of the reservoir) and tested for significantdifferences using two-way ANOVA . Note that positional dif-ferences for streamflow could not be evaluated becausethere is only one active gaging station (located in thedownstream reaches) located in the study area. Onlyinstantaneous streamflow velocity and total suspendedsolids showed significant above/below reservoir effects.During low and moderate flow months instantaneousstreamflow velocity was 25–99% higher at downstreamstations. During four of the five sampling periods whentotal suspended solids were measured, total suspendedsolids were greater above the reservoir than below indi-cating that the reservoir may improve water clarity. Envi-ronmental determinant data (O 2 , total suspended solids,nitrate/nitrite, total Kjeldahl nitrogen, dissolved ortho-phosphorus and total phosphorus), available from aClermont County Office of Environmental Quality spon-sored study of water quality in East Fork (Tetra Tech,2001), were screened for above/below reservoir effects.Comparisons of annual means at Stations EFRM 34.8and 44.1 (upstream) and EFRM 12.7 and 4.0 (down-stream) indicated that only total suspended solids variedsignificantly above and below the reservoir (suspendedsolids were twofold greater above the reservoir). Nutrientlevels on the mainstem of EFLMR below the reservoirincreased with distance from the reservoir and encom-passed the values reported for upstream stations. Total microbial biomass  Total viable microbial biomass in East Fork sedimentsranged between 2 and 134 nmol PLP ã g - 1  dry weight(d.w.) with a mean of 25 nmol PLP ã g - 1  d.w. A one-way ANOVA  indicated that natural log biomass changed signif-icantly with season ( P    <  0.001). Sedimentary microbialbiomass was significantly greater in samples collectedbetween October and December than during any othersampling interval (Table 2, Tukey HSD, a = 0.05). Meanbiomass levels did not vary significantly among samplescollected between January and September. These values Table 1. Nutrient levels at most downstream and upstream monitoring stations of the East Fork Little Miami River. a StationDissolved oxygen (mg l − 1 )Nitrite/nitrate (mg l − 1 )Dissolved ortho-phosphate (mg l − 1 )EFRM0.51996–00 87 8.70 ±  2.40 b 1998–00 47 1.79 ±  0.791996–00 78 0.38 ±  0.19EFRM44.11997–00 67 7.31 ±  1.141998–00 46 0.84 ±  1.071997–00 67 0.87 ±  0.06 a. From Clermont County, Ohio, monitoring programme to characterize the surface water quality of the East Fork of the Little Miami River (TetraTech, 2001). b. Sample period, n  , mean ±  S.D. Table 2. Seasonal changes in water temperature, steamflow velocity and discharge and microbial biomass in the East Fork.Seasonal sampling intervalWater temperature( ∞ C)Instantaneous velocity(ms - 1 )Mean 7-day discharge a (m 3  s - 1 )Microbial biomass(PLP ã g - 1 )Jan–April7.3 b 0.393617May–June230.114525July–Sept.200.121.820Oct–Dec.90.112.234 a. Mean 7-day discharge prior to sampling determined from measurements collected at the USGS Perrintown gaging station. b. Mean value for all samplings occurring during the designated seasonal sampling interval between the years 1996 and 1999.  258 S. D. Sutton and R. H. Findlay   © 2003 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology  , 5 , 256–266 are comparable to stream sediments studied by Bott andKaplan (1985) and, for the most part, fall within the totalrange of values reported for freshwater sediments (7–464 nmol PLPã g - 1  d.w., Dobbs and Findlay, 1993). Multivariate analysis of microbial community structure  We used principal component analysis (PCA) to examinepatterns of variation among PLFA profiles of sedimentscollected throughout the three-year field study (177 sam-ples). Scatter plots of sample factor scores revealed gen-eral patterns of seasonal variation in community structurefor PC1, PC3 and to a lesser extent for PC2 (Fig. 1).Samples with positive PC1 scores (Fig. 1) were enrichedin PLFA with high PC1 loadings ( > 0.5). These fatty acids(10me16:0, a17:0, br17:1a, 17:0, 17:1 w  6/cy17:0, cy19:0,18:1 w  7c, 18:2a, i17:0) are typically present in the mem-branes of heterotrophic bacteria. Conversely, samples withnegative PC1 scores were enriched in the polyenoic PLFAthat had component loadings <- 0.5. With few exceptions,the latter group is restricted to microeukaryote membranesand is typical of phototrophic microeukaryotes (Fig. 1).Comparison of PC1 scores by seasonal sampling inter-val confirmed that the major component of variation incommunity structure was seasonal and reflected changesin the balance between prokaryotic and eukaryotic biom-ass (Fig., 2, Tukey’s HSD, a   =  0.05). Seventy-nine percent of the samples collected between January and Junehad positive PC1 scores indicating that prokaryotes weredisproportionately abundant in these samples comparedto samples with highly negative PC1 scores. Seventy-twoper cent of samples collected between July and Decem-ber had negative PC1 scores indicating that these sam-ples were more enriched in microeukaryotes compared tosamples with highly positive PC1 scores.Although patterns of seasonal variation on PC2 wereless pronounced between January and September, therewas a significant shift in community composition betweenthe July to September and October to December samplingintervals (Fig. 2, panel 2). Phospholipid fatty acid with 18carbons in the aliphatic chain (18:0, 18:1 w  9c and 18:3 w  6)were enriched in samples with highly negative PC2 scores(Fig. 1). PLFA with high PC2 loadings (16:1 w  7c, 16:1 w  9c,i15:0, a15:0, 16:1 w  5c and 14:0) were enriched in sampleswith highly positive PC2 scores (Fig. 1). Patterns of vari-ation in community structure along PC2 were not relatedto sample station position nor were they correlated withwater temperature.Ninety-three per cent of samples collected betweenJanuary and April had negative PC3 scores while 81%of samples collected between May and September hadpositive PC3 scores (Fig. 2). PLFA with high PC3 load-ings (saturated 14-, 15- and 16-carbon fatty acids; Fig. 1)were generally more predominant in samples collectedbetween May and September than in samples collectedbetween January and April. PLFA with low PC3 loadingsincluded 18:1 w  7c and an unidentified dienoic 18-carbonfatty acid and were enriched in samples with highly neg-ative PC3 scores (predominantly January–April samples).Sediment samples collected during the October toDecember sampling interval had intermediate PC3scores. This pattern of variation was moderately positivelycorrelated with water temperature ( R    =  0.685). Fig. 1. Patterns of seasonal variation in sedimentary microbial com-munity composition in the East Fork.A. Scatter plot of sample scores for principal components 1 (abscissa) and 2 (ordinate).B. Scatter plot of sample scores for principal components 1 (abscissa) and 3 (ordinate). PC1 explained 32.3% of the variance and compo-nents two and three explained an additional 17.9 and 17.4% respec-tively. Solid squares represent samples collected between January and April, circles represent samples collected in May and June, triangles represent samples collected between July and September and open diamonds represent samples collected between October and December. Identified fatty acids had component loadings > | 0.5 | and exerted strong influence on the pattern of variation among samples along the respective component axes. AB –4 –3 –2 –1 0 1 2 343210–1–2–3–4–4–3 –2 –1 0 1 2 33210–1–2–3  Microbial community dynamics in stream sediments  259  © 2003 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology  , 5 , 256–266 Changes in microbial community structure by season  During January to June sedimentary microbial biomasswas predominately prokaryotic (60%, Fig. 3A), whilemicroeukaryote biomass was dominant in samples col-lected between July and December. Total microeukaryotebiomass more than doubled between July–Septemberand October–December while there was no significantseasonal variation in total prokaryote biomass (Fig. 3B).Unique community shifts occurred between January–April and May–June samples. Although samples collectedbetween January and April were predominantly prokary-otic, 20:5 w  3/20:4 w  6 ratios were relatively high suggestinga seasonal peak in diatom abundance (Fig. 4, panel 3).May–June and July–September samples showed a sig-nificant decrease in 20:5 w  3/20:4 w  6 ratios indicating adecreased importance of diatoms during this period.Conversely, the microeukaryote component as a wholeshowed a proportional increase during these warm-watermonths (Fig. 4 panel 3 versus Fig. 3A).Many samples collected during the May–June samplinginterval were enriched in saturated PLFA. These included16:0 and 14:0, which are broadly distributed among manytypes of microorganism, as well as two fatty acids that arebroadly distributed among prokaryotes (15:0 and 17:0).Other influential PLFA included i15:0 and i16:0. Together,this group of PLFA represents Gram-positive prokaryotesand facultative Gram-negative bacteria (Kaneda, 1977;Parkes and Taylor, 1983; Edlund et al  ., 1985; Guckert et al  ., 1985). These data suggest that during warm-watermonths there was a persistence (or perhaps emergence) Fig. 2. Seasonal patterns of variation in sedimentary microbial com-munity structure determined by PLFA analysis. Mean factor scores for samples grouped according to seasonal sampling interval. The top panel is a summary for PC 1, the middle panel for PC 2 and the bottom panel for PC3. Vertical error bars represent the 95% confidence inter-val around the means. Letter designations at the top of each panel correspond to the bar below and indicate homogenous subsets iden-tified by Tukey’s HSD ( a   = 0.05). Bars identified by different letters are significantly different, whereas those with the same letter are not.–0.5–1.0–1.5 Jan.–Apr. May–June July–Sept. Oct.–Dec. –––––– Fig. 3. Seasonal variation in microeukaryote and prokaryote biom-ass in East Fork sediments. Samples are grouped according to sea-sonal sampling interval. In A, bars represent the mean percentage total biomass (as g Carbon). In B, bars represent the mean microbial biomass (calculated as mg C·g - 1  d.w.) of the two phylogenetic groups in each sampling interval. In A and B, open bars represent the total microeukaryote biomass and solid bars represent the prokaryotic component. Vertical error bars represent the 95% confidence interval around each mean. Carbon biomass was estimated from PLP and PLFA as described in Dobbs and Findlay (1993).

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