bioremediation of aquaculture wastes

Available online at www.sciencedirect.com

Bioremediation of aquaculture wastesPamela Chavez-Crooker1,2 and Johanna Obreque-Contreras1

Environmental impacts of wastes from large-scale, intensive

aquaculture are substantial and can lead to complex

ecosystem changes. The application of known and new

technologies can capture inorganic nitrogen from water and

reduce organic enrichment of sediments. Biological methods,

including Integrated Multi-trophic Aquaculture are now gaining

interest for increasing in situ removal of nitrogen and other

nutrients at sea cage sites. Several studies on biological

nitrogen removal through nitrification, denitrification and

anaerobic ammonium oxidation (anammox) have been

reported and a number of bacterial groups active in this regard

have been described. Nevertheless, additional efforts need to

be focused on remediation of aquaculture wastewater and

marine sediments. Conventional treatment systems have

several disadvantages. Development of more efficient reactor

systems and a holistic, integrated approach to waste treatment

would allow more environmentally balanced aquaculture

practices.

Addresses1 Biotecnologıas Aguamarina S.A., Esmeralda 1807 of. 101, Antofagasta,

Chile2 Instituto de Biotecnologıa de Tarapaca (IBT), Universidad Arturo Prat,

Cordunap, Avenida Playa Brava 3256, Iquique, Chile

Corresponding author: Chavez-Crooker, Pamela

([email protected])

Current Opinion in Biotechnology 2010, 21:313–317

This review comes from a themed issue on

Evironmental biotechnology

Edited by Sharon Borglin and John van der Meer

Available online 27th April 2010

0958-1669/$ – see front matter

# 2010 Elsevier Ltd. All rights reserved.

DOI 10.1016/j.copbio.2010.04.001

IntroductionThe global growth of aquaculture industries has brought

an increase in negative environmental impacts through

the discharge of substantial amounts of polluting effluents

containing uneaten feed and feces. This organic enrich-

ment causes environmental deterioration of both the

receiving water bodies and sediments [1�]. The initial

effect of adding large amounts of decomposable organic

waste to marine sediments is increased metabolic activity

by aerobic bacteria. Their demand for oxygen results in

localized hypoxia or anoxia, killing the most susceptible

aerobic life forms [2]. In the case of sediment in fish-cage

footprints, much of the continuing metabolism then

www.sciencedirect.com

proceeds by anaerobic sulfate reduction [3]; simul-

taneously, the lack of oxygen inhibits aerobic nitrification

and denitrification processes [4]. Lack of sufficient ox-

ygen leads to the death or migration of the sediment

macrofauna responsible for bioirrigation, and thus to a

decline in aerated water within sediments and a further

spread of anoxia. Upon the loss of bioirrigation, pelagic–benthic coupling becomes reduced for these anoxic, azoic

sediments. The net effect of organic enrichment in

sediments is to move the ecosystem to the one dominated

by bacteria, ciliates and meiofauna, where the trophic

links to the next level of the food web are broken [5–7].

Under these conditions, the predominant bacteria are

anaerobes, mainly sulfate reducers and methanogens

[5]. Pohle et al. [8] reported one study of benthic–pelagic

coupling for salmon aquaculture. Although cause and

effect are not yet well established, it seems probable that

organic enrichment impacted this coupling in a way that

excluded some species and encouraged others.

Organic enrichment also can lead to an increased pre-

sence of pathogenic bacteria. Studies on surface sedi-

ments of a well-established fish farm showed that benthic

bacteria levels were closely related to organic enrichment

and their concentration was three times higher in stations

beneath the cages. Counts (colony forming units (CFU))

of heterotrophic bacteria indicated a shift toward Gram-

negative bacteria, with a predominance of Cytophaga/

Flexibacter-like bacteria (CBF), and the occurrence of

pathogenic bacteria (such as Vibrio) in sediments beneath

the cages. In contrast, Gram-positive bacteria were more

prevalent in the control site, where they represented up to

90% of total isolates [6].

Sediments close to aquaculture facilities can become

enriched reservoirs of viruses associated with organic

detritus [9]. Labrana et al. [10] showed that IPNV in

Chilean salmon farms can remain active in fresh water

sediments for weeks and that the virus can be detected in

areas with a previous history of IPNV outbreaks. Also,

examples are known from shrimp aquaculture where

water and soil from the cultivation ponds contributed

importantly to the spread of viruses to neighboring ponds

or farms [11].

In view of the potential environmental impacts as well as

economic impacts through disease transmission, it is

relevant to suggest that improvement in aquaculture

waste management is a highly desirable objective.

Removal of nitrogen and phosphorus from the water

column to mitigate eutrophication along with improved

wastewater and sediment treatments that reduce the level


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http://dx.doi.org/10.1016/j.copbio.2010.04.001

314 Evironmental biotechnology

of organic matter thereby, biological risk, will do much to

make aquaculture a sustainable farming practice for the

long term.

Treatment of wastesBioremediation of water and sediments contaminated by

sea cage aquaculture, and of effluents discharged by land-

based aquaculture activities, brings into play many organ-

isms, including bacteria, microalgae and macroalgae. For

sea cage operations, bioremediation techniques con-

ducted on-site are likely more feasible than land-based

treatments. However, for some aquaculture operations a

combination of standard waste treatment methods and

other bioremediation techniques may be needed [12,13].

Integrated Multi-trophic Aquaculture

Integrated Multi-trophic Aquaculture (IMTA) strategies

[14] have been described as a key development for

aquaculture sustainability [15–17]. IMTA integrates a

number of complementary organisms at a farm site in

order to optimize nutrient utilization and reduce solid

waste that goes to sediments. The waste from one organ-

ism becomes a source of energy for others, thereby mov-

ing toward a better ecosystem balance [17]. Valuable

seaweeds strip ammonium, nitrate and phosphorous

excreted by fish from the water column, simultaneously

gaining nutrients for growth and removing aquaculture

pollutants. Shellfish and other filter feeders convert sig-

nificant amounts of particulates from uneaten fish feed

and feces into harvestable body biomass. Bottom feeders

can also be integrated into the system to help work

sediments, removing organics and enhancing bioirriga-

tion. Although IMTA may not remove all inorganic and

organic waste from aquaculture farms, combining this

approach with biotechnological applications such as inte-

grated anaerobic–aerobic reactors for waste treatment

need to be investigated at industrial pilot scale [18,19��].

Microbial nitrification and denitrification in sediments

Biological nitrification: Under aerobic conditions, two

groups of bacteria convert ammonium to nitrite and then

to nitrate (NH3–NO2�–NO3

�). This is a process that

consumes a great deal of oxygen and can lower dissolved

oxygen in the area. The aerobic ammonia-oxidizing bac-

teria (AOB) oxidize ammonia to nitrite via hydroxylamine

and then the nitrite-oxidizing bacteria (NOB) oxidize

nitrite to nitrate. The AOB are frequently combined with

another group, the ammonia-oxidizing archaea (AOA),

known together as the ammonia-oxidizing microorgan-

isms (AOM) [20–22]. Autotrophic bacteria in these groups

use the reducing power of the nitrogenous substrates to

fix CO2 via the Calvin–Benson cycle as their source of

carbon. The ammonia oxidizers belong predominantly to

the b-subclasses and g-subclasses of the Proteobacteria

[23], whereas the nitrite oxidizers belong to the a-sub-

classes and g-subclasses of the Proteobacteria and the

phylum Nitrospirae [24]. Not surprisingly, the nitrate and


ammonia serve as principal nitrogen sources for the

growth of some microorganisms.

Biological denitrification: Denitrification is the main mech-

anism for converting fixed nitrogen to N2 gas, which

returns to the atmosphere. It occurs under low oxygen

conditions, in energy-generating reactions where oxides of

nitrogen, including nitrate, nitrite, and nitric and nitrous

oxides, are used as electron acceptors in place of oxygen,

finally becoming reduced to N2 gas as the end product

[25�]. A broad spectrum of microorganisms is capable of

denitrification reactions, including various bacteria,

Archaea and Eukarya [26�,27,28]. Known denitrifying bac-

teria and archaea possess several clusters of genes involved

in denitrification [29�]. These genes encode four metal-

loenzymes: nitrate reductase, nitrite reductase, nitric oxide

reductase and nitrous oxide reductase, which sequentially

reduce nitrate to N2 (NO3�, NO2

�, NO�, N2O, N2) [29�].

Anammox: Anaerobic ammonium oxidation is another

route to denitrification. It was first discovered in anoxic

(denitrifying) bioreactors of wastewater treatment plants

[30], where novel organisms related to Planctomycetales

were found to be capable of oxidizing ammonium using

nitrite as electron acceptor [26�]. First thought an oddity,

it was later found that anammox was responsible for 24–67% of nitrogen loss in marine sediments [31]. Anammox

activity now appears to account for 20–40% of all nitrogen

loss in the ocean [32–36]. It is also present in coastal and

estuarine sediments [26�,31,37–40], anoxic basins [33,34],

oxygen minimum zones [35,36,41,42], mangroves [43],

sea-ice [44] and freshwater lakes [45]. It seems likely that

anammox activity would be a major contributor to deni-

trification of anoxic aquaculture-derived sediments.

Technological applicationsLand-based aquaculture and biological filters

Environmental impacts are minimized by taking aqua-

culture operations onto land where waste products can be

accessed more readily. For flow-through systems the gain

is marginal as large volumes of wastewater are still dis-

charged into a receiving water body. However, for recir-

culating systems, the volume of the waste streams

becomes more manageable and various treatment options

can be considered.

Protein is the major component of fish feed, and is used by

fish for both growth and energy production. During

protein metabolism, ammonium, which is toxic to fish,

is generated as an end product [1�]. To maintain good

water quality, recirculating systems use biological filters

in which heterotrophic bacteria break down organic

wastes and aerobic nitrifying bacteria convert ammonium

to nitrate which is eventually discharged in the waste

stream. Maintaining biological filters requires care as the

bacteria responsible for ammonium oxidation are very

sensitive to operating conditions, particularly pH. For


Bioremediation of aquaculture wastes Chavez-Crooker and Obreque-Contreras 315

larger aquaculture operations, it becomes feasible to

construct an on-site, dedicated wastewater treatment

facility to remove the nitrate and treat solid wastes before

release to the environment.

Treatment of aquaculture wastewater: A wide range of

physical, chemical, and biological processes can contrib-

ute to the removal of nitrogen from wastewater in bio-

logical treatment systems. Treatment facilities and

reactors take on many designs. All use processes that

are derived from an integration of various components of

the natural biogeochemical cycling of nitrogen in the

environment; however, they are operated so as to maxi-

mize the kinetics of the activities during remediation

treatments. A treatment system that combines total

microbial nitrification with anammox (to reduce nitrite)

seems to be more cost effective than most others [46��].The desired reactor configuration depends on the waste

characteristics such as the concentration of organics and

ammonium. In all cases, the key step appears to be partial

nitrification [47]. Processes that use partial nitrification or

combine partial nitrification with anammox in suspended

biomass or biofilm reactors have been developed, in-

cluding a new process that is based on anaerobic ammonia

oxidation coupled to conversion of nitrate into nitrite,

driven by sulphide [48]. More studies are needed on

microbial processes controlling nitrogen removal in

immobilized systems such as biofilters or biofilms and

in wetlands used for the bioremediation of wastes [49].

Wetlands are sometimes linked to recirculating aquacul-

ture systems as a final treatment phase before complete

release of effluents to the environment. In one test of such

a wetland system, small-scale treatments of effluents from

a trout farm were conducted using a constructed wetland

with subsurface flow. With loading rates involving large

volumes of water, and consequently, short retention

times, wetland treatment of dissolved nutrients was effec-

tive only for the ammonium and nitrites while nitrate and

phosphate showed no, or even negative, treatment effects

through the wetland passage [50]. More effective removal

of the nitrogen could be expected with longer retention

times.

Some examples for nitrogen removal in aquaculture sys-

tems using simple in situ biological reactors have been

reported. Kumar et al. [51] described a rapid setting up of

nitrification using ammonia oxidizers (native and exogen-

ous strains) in stringed bed suspended bioreactors

(SBSBR) in a shrimp hatchery. De Scheryver and Ver-

straete [52] reported the potential of batch reactors

(SBRs) as an alternative bio-flocs technology approach

in aquaculture. Manju et al. [53] reported immobilized

nitrifying bacterial consortia as bioaugmentators for in situapplications in shrimp aquaculture. Lyles et al. [54]

reported a biological treatment (SBRs) for shrimp aqua-

culture wastewater.


ConclusionsThe aquaculture industry, especially intensive salmon

aquaculture in near-shore waters, is facing an important

challenge in maintaining social, economic and environ-

mental sustainability. Recently, in Chile, a single disease

caused the loss of millions of dollars and thousands of jobs

through the closure of hundreds of production centers.

The role of waste management, or the lack thereof, is not

known in this instance; however, it demonstrates the scale

of costs associated with outbreaks that could be derived

from pathogens harbored in waste sediments. Several

strategies and treatment technologies are being available

for enhanced aquaculture waste treatments and for in situremediation strategies. The aquaculture industry needs

to consider these carefully and integrate better waste

management into their operations as an investment that

will help them sustain and augment their production

while still protecting the environment.

AcknowledgementsWe would like to thank the Chilean Government for support throughCONICYT and FONDEF Grant DO8I1027. A special thanks goes to DrThierry Chopin for providing copies of reprints relating to IMTA used forthis manuscript.

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