The role of microbial populations in the cycling of iron and manganese from marine aggregates

Abstract

Marine aggregates play an important role in the cycling of carbon, nutrients and trace
metals. Within aggregates the oxygen depleted by aerobic microbial respiration may
not be replaced rapidly, generating anoxic or suboxic microzones. Reduced
compounds that are unstable in the oxygenated water column have been previously
found associated with marine snow. Therefore, in the experiments described in this
thesis, artificial aggregates were made in the laboratory from senescent phytoplankton
material and incubated to investigate the role of the associated microbial populations
to the biogeochemical redox cycling of iron and manganese and to the degradation of
organic matter.
The release of dissolved iron from artificial aggregates which did not contain any
measurable (~10 ?m) anoxic microzones, was demonstrated under dark conditions.
The rate of release was controlled by the amount of reducible Fe(III) available, and
appears to be limited by the competing oxidation of Fe(II). Moreover highly significant
releases in reduced Mn were detected from aggregates incubated under a constant
velocity shear, although the same aggregates did not affect the dissolution of iron. A
possible reason is likely associated with the higher stability of Mn(II), compared to
Fe(II) in aerobic environments.
Molecular (16S rRNA gene) analyses showed the bacterial community
associated with artificial aggregates to be similar to that found in natural aggregates
and dominated by (predominantly uncultured) ?- and ?-Proteobacteria, Bacteroidetes,
Planctomycetes and Cyanobacteria. It was possible to culture NO3
--, Fe(III)- and
Mn(IV)-reducing bacteria from the artificial aggregates, and marine particles incubated
with Fe(III) under anaerobic conditions contained a range of ?- and ?-Proteobacteria
known to respire Fe(III) and in most cases Mn(IV). Moreover several microorganisms
belonging to ?-Proteobacteria were isolated from marine aggregates and strains
affiliated to the genera Amphritea, Marinobacterium and Marinobacter, were
demonstrated to grow through the reduction of Fe(III), with Marinobacter also capable
of respiring Mn(IV). Whilst the precise mechanism of reduction is not clear, it is evident
that marine aggregates can be a source of Fe(II) and dissolved Mn, in coastal waters
and most probably other natural water systems.
Fatty acid analyses revealed the prevalence of saturated over unsaturated fatty
acids indicating that aggregates were already partially degraded when incubation
started. Nonetheless, the lipids in the artificial aggregates were rapidly degraded
further as indicated by a depletion in short chain (<20) saturated and
monounsaturated fatty acids. In contrast, the concentrations of linear and branched,
saturated long chain (>20) fatty acids fluctuated, suggesting that some of these lipids
could have been produced in situ by marine microorganisms rather than deriving from
II
higher plant debris. In addition, a bacterial branched monounsaturated fatty acid (11-
methyl-octadecenoic acid), which has not previously been found in marine particles
was present in artificial aggregates. Roseobacter litoralis found among the aggregateattached
bacteria contains 11-methyl-octadecenoic acid, and other bacteria present in
artificial aggregates have the potential to produce long-chain saturated and
polyunsaturated fatty acids. Thus, the fatty acid assemblage appears to reflect both
organic matter degradation, including selective preservation, but also changes in the
microbial assemblage.
A range of future studies are suggested to elucidate the mechanisms for Fe(III)
and Mn(IV) reduction in aggregates. These include microscale analyses of dissolved
species and evaluation of the presence of metal binding ligands associated with
aggregates. Moreover it is important to assess the activity of the Fe(III)- and Mn(IV)-
reducing bacteria present in aggregates in situ and the production of long chain fatty
acids in degrading aggregates.

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