Plant Molecular Biology 41: 89–104, 1999.
© 1999 Kluwer Academic Publishers. Printed in the Netherlands.
Expression of photosynthesis genes in relation to nitrogen ﬁxation in the
diazotrophic ﬁlamentous nonheterocystous cyanobacterium
Trichodesmium sp. IMS 101
, Benny Dominic, Sabino Zani, Mark T. Mellon and Jonathan P. Zehr
Biology Department, Rensselaer Polytechnic Institute, 110 8th Street, Troy, NY 12180-3590, USA; current
Institute of Marine and Coastal Sciences, Rutgers University, 71 Dudley Road, New Brunswick,
NJ 08901, USA;
Ocean Sciences Department, University of California, 1156 High Street, Santa Cruz, CA 95064,
author for correspondence)
Received 9 December 1998; accepted in revised form 2 July 1999
Key words: cyanobacteria, circadian rhythm, psaA, psbA, Trichodesmium sp.
The daily cycle of nitrogenase expression in the marine ﬁlamentous nonheterocystous cyanobacterium Tri-
chodesmium spp. is controlled by a circadian rhythm. We evaluated the rhythm of two key photosynthesis genes,
psbA of photosystem II and psaA of photosystem I, in Trichodesmium sp. IMS 101 using the 3 criteria for an
endogenous rhythm. The transcript abundance of psbA and psaA transcripts oscillated with a period of ca. 24 h
under a 12 h light/12 h dark regime. At 24
C and 28
C the cyclic pattern of transcript abundance was maintained
for at least 58 h under constant light conditions, whereas the periods were about 24 h at 24
C, and 26–30 h
at the higher temperature. The cycles of psbA and psaA gene expression were entrained using light-dark cues.
Transcription of nifHDK was initiated prior to the light period, followed by psbA and ﬁnally psaA.Therewas
(6 h) phase difference between the net accumulation of nifHDK and psbA transcripts, as well as between
that of psbA and psaA transcripts. Results of inhibitor experiments indicated that psbA and psaA transcription was
regulated differently by initiation and degradation during the light period. Short-term changes of light conditions
resulted in signiﬁcant effects on psbA transcription and nitrogenase activity, but had less of an effect on psaA and
Trichodesmium spp. are diazotrophicﬁlamentous non-
heterocystous marine cyanobacteria. Trichodesmium
contributes signiﬁcantly to the annual input of new ni-
trogen to the nutrient-limited surface waters of tropical
and subtropical oceans all over the world (Carpenter,
1983; Gallon et al., 1996; Capone et al., 1997; Zehr
et al., 1998). Trichodesmium ﬁxes nitrogen exclu-
sively during the light when oxygenic photosynthesis
is concurrent, without any known mechanism to either
temporally or spatially separate oxygenic photosyn-
The nucleotide sequence data reported will appear in the
EMBL, GenBank and DDBJ Nucleotide Sequence Databases under
the accession numbers AF107784 (psbA) and AF107783 (psaA).
thesis from oxygen-sensitive nitrogen ﬁxation. How
Trichodesmium protects nitrogenase from inactivation
by oxygen is a perplexing and fascinating question.
In the past, relatively few studies have focused on
photosynthesis by Trichodesmium. Based on parallel
ﬁxation measurements, it was sug-
gested that the patterns of photosynthetic CO
in both cultured and natural Trichodesmium popula-
tions were similar and corresponded over time to the
patterns of N
ﬁxation (Paerl, 1994). Microautora-
diographic data from the same study also provided
some evidence of a possible spatial separation be-
tween carbon and nitrogen ﬁxation (Paerl, 1994).
Results of studies using immunohistochemistry cou-
pled with light and transmission electron microscopy