1542

Limnol. Oceanogt’., 33(6, part 2), 1988. 1542-1 55X

O 1988, hy the American %cicty of Limndogy and oceanography, Inc.





Contribution of bacteria to release and fixation of

phosphorus in lake sediments

Renk Gachter, Joseph S. Meyer, and A ntonin Mares

Institute of Aquatic Sciences, Swiss Federal Institute of Technology (ETH),

Lake Research Laboratory EAWAG/ETH, CH-6047 Kastanienbaum



Abstract

Cycling of phosphorus at the sediment-water interface is traditionally considered to bc controlled

by pH- and rcdox-dependent, abiotic processes, such as formation and dissolution of FeOOH-POd

complexes. In this study, however, a large part of total P in sediments of Lake Sempach, an 87-m

deep eutrophic lake, was estimated to bc incorporated in bacterial biomass. Laboratory experiments

indicated that sediment microorganisms can rapidly take up and release soluble reactive P (SRP),

depending on rcdox conditions, and that sterilization ofoxic sediments decreased their SRI? sorption

capacity. In an in situ experiment conducted in the lake, bacteria also contributed considerably to

SRP fixation when water enclosed within a sediment flux chamber was reoxygenated following

anoxia, Moreover, in that experiment and in data sets from several other lakes, anoxic releases of

Fc and P from sediments appeared to be partly uncoupled. As part of an ongoing revision of the

classical model for P exchange across the sediment-water interface, these results provide direct

cvidencc that fixation and release of SRP may be controlled part! y by rcdox-dependent changes

a

in microbial physiology, s Wellas by productionand dc~ornmsitionOfmicrobial biomass.









In addition to external loading and loss organisms only play an indirect role by con-

through the outflow, net sedimentation af- suming Oz and N03 - during organic matter

fects the cycling of phosphorus in lakes. The decomposition, thus providing necessary

sediment-water interface may act either as conditions for abiotic or biotic reduction of

a permanent sink or as a transient source Fe(III) and subsequent release of POz3-

for P. According to classical theory based (Jansson 1987).

on studies of Mortimer (1941, 1942) and Although numerous field and laboratory

Einsele. ( 1936), P flux at the sediment-water studies support the classical model, it has

interface is controlled primarily by ferric not yet been clearly demonstrated in any

iron [Fe(ITI)], to which POd3’- adsorbs to lake that a substantial part of the POQ3- re-

form solid FeOOH-POo complexes. Mor- leased under anoxic conditions was previ-

timcr (1941) mentioned the possibility and ously bound to Fe(III). 13ased on results from

Davison and Tipping (1984) provided evi- recent laboratory experiments and studies

dence that organic constituents also form a conducted in shallow lakes, Bostri5m et al.

part of the POA3--adsorbing ferric complex. (1982, 1988) discussed additional physical

When hypolimnetic water becomes anoxic and chemical mechanisms controlling P cy-

and sediment redox potential decreases, cling at the sediment-water interface. They

these ferric complexes dissolve, and Fe and especially emphasized -that living In icroor-

POd3- are released into the hypolimnion. In ganisms can play a direct role by acting as

this traditional model, sedimentary micro- either a sink or a source for P043-. In deep-

water lakes, however, evidence for similar

AcknowIedgments biotic uptake and release controlling P cy-

This material is based, in part, on work supported cling is limited.

by the North Atlantic Treaty Organization .undcr a Lake sediments are complex systems, and

grant awarded to J.S.M. in 1987. The comments of P.

Bossard, J. Shapiro, R. Schwarzenbach, and E. Laczko it i.s not easy to separate the contribution of

in reviews of an early version of the manuscript are microorganisms to either fixation or pro-

appreciated. We especially thank C. H. Mortimer, B. duction of P043- from the postulated abiot-

Bostrom, and R. E. StaulTer, whose comments and ic coupling between Fe and P cycles. For

suggestions helped to clarify and improve this paper.

H. Ambuhl, M. Schmid, and A. Stoeckli provided un-

this reason, we conducted laboratory ex-

published Fe and P concentrations from Lake Hallwil periments with cultures of sedimentary bac-

and Greifensee. teria and with sterilized secliments, i.n order

1542

m









Bacteria and P in sediments 1543



to identify conditions under which sedi- mann (1955) and Wagner (1969), respec-

mentary microorganisms might contribute tively. Oz, Ca2-’(complexometric titration),

to POd3- uptake and release. We also con- and pH were analyzed according to Deutsche

ducted an in situ experiment with bottom Einheitsverfahren zur Wasser-, Abwasser-

water to test whether microbial processes und Schlammuntersuchung (VCH Ver-

observed in the laboratory contribute con- lagsges.). Concentrations of dissolved (DFe

siderably to P fluxes across the profundal and DMn) and total (TFe and TMn) Fe and

sediment-water interface. Finally, we mea- Mn were determined by graphite furnace

sured bacterial biovolume in sediment from atomic absorption. Concentrations of par-

Lake Sempach, an 87-m-deep, eutrophic ticulate Fe and Mn (PFe and PMn) were

lake in north-central Switzerland, and es- calculated as the difference between their

timated the amount of P incorporated in respective dissolved and total concentra-

bacteria. Our results show that the apparent tions. Samples for DFe and DMn were fil-

simultaneous release of Fe and POQ3-from tered immediately after collection and acid-

anoxic sediments is not conclusive proof ified with HC1 to about pH 3,

that the two elements were associated before Wet sediments were dried to constant

the onset of anoxia, as is assumed in the weight at 80”C for percent moisture analy-

classical model. Furthermore, in some deep- ses. POC analysis of wet sediment was the

water lakes, Fe and POA3-are not even re- same as described for aqueous samples. Cal-

leased simultaneously into bottom water. cium in dried sediment was determined by

These findings suggest that in sediments of complexometric titration after combustion

deep-water eutrophic lakes, microorgan- (550”C) and dissolution in HC1. After acidic

isms responding to variations in redox po- digestion of dried sediment (HJ30JHz02

tential and nutrient concentrations may also at 260”C), TFe, TMn, and TP were deter-

contribute considerably to uptake and re- mined as described for the aqueous proce-

lease of P. dure.

Laboratory experiments with sedimentary

Methods microorganisms – Two identical experi-

Chemical analyses–Unless stated oth- ments were conducted about 1 month apart

erwise, all filtered samples were passed in fall 1986. In each experiment, culture

through 0.45-~m Sartorious CA membrane medium containing 6.7 g of standard 1 nu-

filters. Soluble reactive P (SRP) was deter- trient broth (Merck), 10 g of glucose, and

mined after filtration, according to Vogler 2.7 g of NHaCl was prepared in 10 liters of

(1965). Concentrations of total P in unfil- lake water, then filtered (0.2-~m Sartorius

tered (TP) and filtered samples (DP) were CA membrane filter) and sterilized at 120”C

determined by the same method after diges- for 20 min. After cooling, the medium was

tion with K&Og at 120”C for 2 h. The con- bubbled with air and inoculated with 100

centration of particulate P (PP) was calcu- mg of surface sediment collected at 87 m in

lated as the difference between TP and DP. the lake. When the approximately 150 ~mol

Dissolved organic C (DOC) was analyzed liter-l of SRP in the medium was exhausted,

in filtered water with an autoanalyzer the culture was subdivided and placed in

(Technicon). To determine particulate or- two glass carboys. To one carboy about 10

ganic C (POC), we filtered samples through ~mol liter-’ of PFe in the form of freshly

Whatman GF/F glass-fiber filters (preheat- precipitated FeOOH floes was added; noth-

ed to 500”C). The filters were then moist- ing was added to the other carboy. Since

ened with 1 M HC1 and dried at 40°C to little SRP was in solution at that time, the

remove inorganic C before analysis in a added Fe was unable to bind large amounts

Heraeus CHN analyzer (CHN Rapid). Total of SRP. The cultures in both carboys were

inorganic C (TIC) was calculated from pH then bubbled with Nz gas for about 3 d, after

and alkalinity measurements according to which they were again aerated. SRP, TP,

Harvey and Rodhe (1955). DP, DFe, TFe, POC, and pH were mea-

NO~- and NHa+ in filtered water were de- sured frequently during the first 8 h of an-

termined as described by Miiller and Wide- oxia and oxia and later at daily intervals.

1544 Gachter et al.



4 2 6 In situ experiment with jlux chamber–

u I On 3 .June 1986, a flux chamber was lowered

5 1 ~.A. .

. ontc) the sediment surface at 87 m in the

I I lake. The flux chamber (Fig. 1) is a large

‘t 4 stainless-steel cylinder (1. 5-m diam) with a

lid that closes after the chamber reaches the

sediment surface. When fully implanted in

the sediment, it encloses 440 liters of over-

lying water. Water enclosed within the

chamber is continuously circulated with a

pump at a flow rate of 5.3 liters rein-1 to

ensure uniform mixing; no visible resus-

Enlargement of Section A pensicm of sediment occurs at this low mix-

-—————-—-—-—--——--.-—-—_ - ing rate. Molecular oxygen can be added to

i

I the water by diffusion when 50 cm of Tygon

6 tubing in-serted in the recirculation loop is

I

inflated with pressurized Oz supplied from

I

the lake surface (Fig. 1, enlargement). When

I

Oz pressure in the Tygon tubing is decreased

L–––___–_– –––_–_-–-_–___i

below the hydrostatic pressure in the flux

Fig. 1. Schematic presentation of sediment flux

chamber (enlargement shows Tygon tubing used to add cham”ber, the tubing compresses and no Oz

oxygen). 1—Pump to circulate waler through flux diffuses into the circulating water.

chamber; 2 —tubing for sampling 3--sampling pump; Water samples from the flux chamber

4–tubing to add formaldch yde to sampling tube; 5 – were collected at about daily intervals by

one-way valves; 6 —tubing for supply of pressurized

pumping them to the lake surface through

oxygen; 7 —stoppers; 8—inflated Tygon tubing.

carefully rinsed Tygon tubing. We prevent-

ed growth of bacteria in the tubing by filling

Laboratory experiment with sterilized it with a 40/0-formaldehyde solution between

sediment —The upper 1 cm of sediment was samplings. Fluxes of chemical species

collected from about 10 cores taken on 2 through the sediment–water interface were

September 1987 at 85 m in the lake. Ten calculated from changes in concentration in

grams of homogenized sediment were di- the overlying water, the volume of the en-

luted with filtered hypolimnetic water (0.2- closed water, and the surface area of sedi-

pm Sartorius CA membrane filter) contain- ment enclosed by the flux chamber.

ing 200 ~g SRP liter-1 to a volume of 450 Estimating microbial biovolume –For

ml in each of 12 1-liter bottles. Then 50 ml each aqueous sample, 100 ml of water were

of Formal in were added to six of the bottles pumped directly from the flux chamber into

and 50 ml of distilled H20 to the other six, a sterile 125-ml serum bottle and kept in

producing a 40/0 formaldehyde concentra- the dark in a cooling box. About 2 h after

tion in the sterilized treatments. These sed- collection, acridine orange was added to the

iment suspensions were aerated overnight bottle; 30 min later, aliquots were filtered

at 20°C on a rotary shaker. Five bottles in through 0.2-pm Nuclepore filters prestained

each series were then spiked with additional with Sudan Black B. Fluorescing bacteria

POq3- (as KHZPOJ at O, 800, 1,200, 1,600, were counted with an epifluorescence mi-

and 2,000 pg P liter-1. T“he sixth bottle in croscope and grouped into the following size

each series was spiked with 2,000 ~g P li- classes: rods (range of diameter, range of

ter- 1plus 200 mg C liter-’ (as glucose) and length expressed in ~m) 0.25-0.5, 0.25-0.5;

40 mg N liter-’ (as NHAC1). Aeration and 50V0 of the Fe precipitate dissolved si-









‘fad%aa

0 140

0 0

L!_f’- 140

multaneously with the increase of SRP. The

culture with added FeOOH floes and the

control without such a precipitate released

SRP at equal rates in both experiments.

When air was again bubbled through the

cultures, all of the released SRP was im-

iYME & ;ME ~g)

mediately (1.02 16 >53

0.5-1 9.6 72.1 74.7 1.10 10.8 1.8 265 13.0 0.88 17 80

1-2 10.1 30.5 63.7 0.82 14.1 1.4 257 5.5 0.37 9 45

2-3 10.5 25.1 64.4 0.78 16.1 1.2 250 4:5 0.31 7 40

3-4 13.4 12.5 52.7 0.69 13.5 1.1 245 2.2 0.15 4 22

_—. —

* Dry weight expressed as percentage of fresh weight.

t POC associated with bacteria (abacterial biovolumc x 0.18 mg POC mm-’).

* TP associated with bacteria [=Biu POC x 0.068 mg PP (mg POC)-’].





mentary bacterial composition.. Specifical- Bacteria can also act as a sink or a source

ly, if the larger filamentous forms that of POa:3-, however, and thus play a more

clomin.ated the biovolume of the surface- direct role in uptake and release of P in

sediment community contained consider- sediments. Levine and Schindler (1980)

ably less PP per unit of biovolume than Lean (]. 984), and Currie and Kalff (1 984)

bacteria in the enclosed water (dominated presented experimental evidence that bac-

by nonfilamentous forms), then the esti- teria may outcompete phytoplankton in the

mated percentage of Bio PP would decrease. uptake of SRP, especially at low SRP con-

centrations. Thus, it is not surprising in our

Discussion experiment that sedimentary microorgan-

Despite lack of replication in the sedi- isms depleted SRP concentrations from

ment sterilization and flux chamber exper- >100 ~~mol liter-’ initially to 2.5: 1 in Fe-P precipitates based on figure reductive dissolution of Fe(X3H-P04 com-

4 of Tessenow (1974). Yet the observed plexes should initially result in simulta-

APFe: APP ratio during the first day of the neous, stoichiometric Fe and P releases, un-

subsequent oxic period equaled only 1.4:1, less redox potential is already low enough

and all of the points in Fig. 5 plot well below for formation of insoluble FeS. At first. It

the 2.5:1 line. Hence, the low PFe: PP, might seem that the accelerated release of

ADFe: ASRP, and APFe: APP ratios ob- P without a concomitant release of Fe could

served in the flux chamber experiment in- be explained by retention of Fe as sulfides

dicate that, apart from formation of Fe-P in the sediment. The accelerated release of

complexes, additional PP-forming mecha- Fe 2 d later (probably at an even lower redox

nisms must be considered in the enclosed potential), however. is inconsistent with this

water. explanation. On the other hand, the sudden

As demonstrated in the laboratory ex- halt in Fe release on 16 June could be ex-

periments with sediment bacteria, an ad- plained by FeS precipitation. From these

ditional possibility for PP formation is up- results, we conclude that accelerated release

take of SRP by microorganisms. In the flux of P between 10 and 12 June cannot be

chamber experiment, DOC released from explained by reductive dissolution of

sediments diffused into the overlying water FeOOH-P04 complexes.

and appeared to serve as substrate for mi- There was no similar 2-d interval be-

crobial production. During the oxic phases tween the increases in SRP and DFe con-

of the experiment, net increases of POC and centrations in enclosed water at the end of

bacterial biovolume were observed, indi- the first oxic period ( 10–12 June). Although

cating that the sediment–water interface is at first this absence might seem to support

not only the place of decomposition of a strong coupling between Fe and P releases

planktonic biomass but that in this layer from the sediment, this result is consistent

there is simultaneous production of micro- with the previous argument because the en-

bial biomass. Since P is an essential nutrient closed water was still oxic on 10 and 11

for all organisms, this biomass production June. SRP diffusing from anoxic sediment

must have been coupled with the formation into the overlying water therefore was prob-

of PP. For example, we estimate that be- ably adsorbed to suspended FeOOH parti-

tween 300/0(based on a minimum PP: POC cles or taken up by bacteria until the water

ratio determined for bacteria in anoxic became anoxic (12 June). Only then could

water: Table 1) and 600/0(based on a APFe: DFe and SRP concentrations increase rap-

APP ratio of 2.5:1 for the formation of par- idly because of redox-dependent release

ticulate Fe-P complexes from the DFe and from bacteria and Fe-P complexes. Thus,

SRP concentrations shown in Fig. 4G) of comparison of concentrations of the two

the PP formed during the 02 pulse following dissolved species (DF”e and SRP) in the en-

the first anoxic period was incorporated in closed water cannot be used to identify their

bacteria. These estimates suggest that bac- sources in the sediment.

teria competed successfully with FeOOH for Dissolution of Mn-P and Ca-P com-

SRP after reoxygenation of flux chamber plexes must also be considered as expla-

1554 Gachter et al.



800 -80



1 s SRP

,a

600- u TFe -60

d’

#







400 “ -40





“*

n *

* a)

200- 8 -20 IL

u









o!

— , m , m ,

n

, m m , 1 . , m , , h

‘J FM AM JJASOND’J FM AM JJASO ND’”



1985 1986

Fig. 6. Concentrations of SRP and TFe in bottom water (45 m) of Lake Hallw il from April to November

1985 and 1986 (M. Schmid and A. Stoeckli unpubl. data).





nations for the early release of P. After lake in northeastern Switzerland) there was

steadily increasing from the beginning of the a 1-month interval between the onset of SRP

experiment until 11 June, however, DMn (April–May) and Fe (May–June) releases in

and TMn concentrations in the enclosed 1985 and a 3-month interval between the

water decreased slightly during the first an- onset of SRP (April–May) and Fe (July–Au-

oxic period (Fig. 4H), just as TP and SRP gust) releases in 1986 (Fig. 7).

releases accelerated. Hence, Mn and P re- There even appeared to be a 10-d interval

leases also appeared to be uncoupled. Sim- between the releases of P20, and Fe [TFe

ilarly, Ca2+ concentration increased most and Fe(II)] in Mortimer’s results for Esth-

rapidly during the initial oxic period, when waite Water at the onset of anoxia during

the release rate of P was at a minimum, and late July and early August 1940 (Fig. 8: re-

then stabilized during the subsequent an- drawn from figure 29 of Mortimer 1942).

oxic period, when the release rate of P was Moreover, based on concentrations for the

at a maximum (Fig. 4B). Thus, dissolution 12 sampling dates from mid-July to mid-

of Ca-P complexes can probably also be dis- October (including the entire period when

counted as a dominant mechanism for P Oz concentration in the sediment and over-

release. lying water was f concentra-

centrations in hypolimnetic waters just tions is not significant. Mortimer (1 942)

above the sediments in several other lakes suggested that the large fluctuations in Fe

support our flux chamber results. For ex- and P concentrations during summer 1940

ample, in Lake Hallwil (a 45-m-deep eutro- were due to unstable conditions in the hy -

phic lake in north-central Switzerland) there polimnion: however. the releases of P~O,

was a 2-month lag in the onset of Fe release and Fe(II) during late July and early August

(July-August) compared to the onset of SRP still should have been synchronous if they

release (May–June) in 1985 (Fig. 6); simi- are to be explained by reductive dissolution

larly in 1986, there was a 3-month lag in of Fe-P complexes. Contrary to the ex-

the onset of Fe release (July–August) com- pected synchrony, P.05 concentration de-

pared to the onset of SRP release (April– creased sharply between 3 and 13 August,

May). In Greifensee (a 30-m-deep eutrophic whereas TFe and Fe(II) concentrations in-

Bacteria and P in sediments 1555



1000 “ “ 200

s SRP



800- n

n

F

o

q -150

I q

’B

a)

@ 600- s -

m=

-

-1oo

y 400-

a)

n “50 IL

200-





o! m 1 # 8 m m m m u I , m m m m . m m m , , m o

JFMAMJJASOND’JF MA MJJASOND



1985 1986

Fig. 7. Concentrations of SRP and TFe in bottom water (30 m) of Greifensee from April to November

. , 1985

and 1986 (H. Ambuhl unpubl. data).





creased (and all Fe was in the reduced form). major part in POQ3- release from Schleinsee

Thus, these results indicate that not all P sediment, although on the basis of those

released from Esthwaite Water sediment was data alone there is no way of testing whether

tightly coupled with Fe. Unfortunately, the microorganisms also contributed directly to

coupling between Fe and P release cannot POq3- release.

be investigated in the 1939 data set for Esth- Another result from the flux chamber ex-

waite Water because P20~ concentration was periment further suggests that Fe and P re-

estimated in only a few water samples (Mor- leases were not completely coupled. During

timer 194 1). the second anoxic period (1-2 July), TFe

Processes occurring in the flux chamber and DFe concentrations increased by about

seem to mimic (at a highly accelerated rate) 40 and 90°/0, indicating that redox potential

processes that naturally occur at the sedi- was low enough for reductive dissolution of

ment–water interface in eutrophic lakes. FeOOH. SRP concentration remained con-

Therefore, on a relative basis, the 2-d lag stant (1 ~mol liter-’) however, and TP con-

between P and Fe releases in the flux cham- centration decreased by 5?A0,contrary to what

ber seems to be equivalent to the lags of might be predicted from the classical model.

several weeks to several months observed

in Lake Hallwil, Greifensce, and Esthwaite 200 -20,000

u P205 (SRP)

Water. All of those observations are con- u

,’ ‘,

s





, 8 TFe

,’ u

sistent with a microbial contribution to .

‘7

,

,

,

s







s

P043- release from sediments, but not all s

,

,

eutrophic lakes exhibit this pattern. For ex- ,

:

# d

ample, no lag between P and Fe releases is ,

,

0.

apparent in data for Schlcinsee during the ,

,

anoxic period in summer 1935 (figures 15

and 16 of Einsele and Vetter 1938), and 0

JUL AUG SEP OCT

there is a high correlation between Fe and

Fig. 8. Concentrations of P,O,, TFe, and Fc(II) in

POa3- concentrations (r2= 0.96, P 500 mg P m- 2 was

in the hypolimnia of oligotrophic Canadian incorporated in bacterial biomass in the up-

Shield Lakes 227 and 302, even though per O.:5 -cm of sediment, given the values

most of the SRP taken up during oxic con- listed in Table 2. Thus, the released P was

Bacteria and P in sediments 1557



equivalent to <400/0 of the bacterial P in the eastern backwater rivers. Limnol. Occanogr. 32:

upper sediment layer. On the basis of results 221-234.

W

EINSELE, . 1936. Uber clie Beziehungen des Eisen-

of our laboratory experiments, sedimentary kreislaufes zum Phosphatkreislauf im eutrophen

bacteria easily could have accounted for a Sec. Arch. Hydrobiol. 29:664-686.

large part of the observed P release. — ANDH. VETTER. 1938. Untersuchungcn uber

Our laboratory and field experiments in- di~ Entwicklung der physikalischen und the-

mischen Verhaltnisse im Jahreszyklus in cinem

dicate that uptake and release of SRP by

massig eutrophen See (Schlcinscc bei Langenar-

bacteria and precipitation and dissolution gcn). Int. Rev. Gcsamten Hydrobiol. Hydrogr. 36:

of FeOOH seem to occur at about the same 285-324.

redox potential. This coincidence might ex- T

FENCHEL, ., ANDT. H. BLACKBURN.1979. Bacteria

plain why direct microbial contributions to and mineral cycling. Academic.

S

FLEISCHER, . 1983. Microbial phosphorus release

uptake and release of P have been over- during enhanced glycolysis. Naturwissenschaften

looked since the very convincing, purely 70:415-416.

abiotic model was proposed more than 40 FLORENTZ,M., P. GRANGER, AND P. HARTEMANN.

yr ago. 1984. Use of 31P nuclear magnetic resonance

spectroscopy and electron microscopy to study

phosphorus metabolism of microorganisms from

wastewaters. Appl. Environ. Microbiol. 47: 519-

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Submitted: 1 May 1987

tionsprozessc in der Oberschicht von Seescdimen- Accepted: 9 March 1988

ten. 4. Reaktionsmechanismcn und Gleichge- Revised: 22 July 1988